Loading…

The antioxidant betulinic acid enhances porcine oocyte maturation through Nrf2/Keap1 signaling pathway modulation

During in vitro maturation, excess levels of reactive oxygen species (ROS) are a major cause of developmental defects in embryos. Betulinic acid (BA) is a naturally produced antioxidant in white birch bark. Recent studies have shown that BA exhibits antioxidant properties in various cells through th...

Full description

Saved in:
Bibliographic Details
Published in:PloS one 2024-10, Vol.19 (10), p.e0311819
Main Authors: Kim, Min Ju, Kang, Hyo-Gu, Jeon, Se-Been, Yun, Ji Hyeon, Jeong, Pil-Soo, Sim, Bo-Woong, Kim, Sun-Uk, Cho, Seong-Keun, Song, Bong-Seok
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by
cites cdi_FETCH-LOGICAL-c506t-b1d565e355f66d059bb0415747ab04492b0b6f6742cb45e41c0ec0e1935e96603
container_end_page
container_issue 10
container_start_page e0311819
container_title PloS one
container_volume 19
creator Kim, Min Ju
Kang, Hyo-Gu
Jeon, Se-Been
Yun, Ji Hyeon
Jeong, Pil-Soo
Sim, Bo-Woong
Kim, Sun-Uk
Cho, Seong-Keun
Song, Bong-Seok
description During in vitro maturation, excess levels of reactive oxygen species (ROS) are a major cause of developmental defects in embryos. Betulinic acid (BA) is a naturally produced antioxidant in white birch bark. Recent studies have shown that BA exhibits antioxidant properties in various cells through the activation of antioxidant genes. Therefore, we investigated the effect of BA treatment on porcine oocytes and its underlying mechanism during oocyte maturation. Treatment with 0.1 μM BA significantly increased the proportion of MII oocytes compared with controls, and BA-treated oocytes had significantly higher development rates, trophectoderm cell numbers, and cell survival rates than controls. These results demonstrate that BA treatment improved the developmental competence of oocytes. Following BA treatment, oocytes exhibited reduced ROS levels and elevated glutathione (GSH) levels, accompanied by the enhanced expression of antioxidant genes, compared with control oocytes. To evaluate the antioxidant effects of BA, oocytes were exposed to H2O2, a potent ROS activator. Impaired nuclear maturation, ROS levels, and GSH levels induced in oocytes by H2O2 exposure was restored by BA treatment. As these antioxidant genes are regulated by the Nrf2/Keap1 signaling pathway, which is involved in antioxidant responses, we applied the Nrf2 inhibitor brusatol to investigate the effects of BA on this pathway. The negative effects of brusatol on meiotic maturation and oocyte quality, including levels of ROS, GSH, and antioxidant-related gene expression, were mitigated by BA treatment. Our results suggested that BA plays an effective role as an antioxidant in porcine oocyte maturation through adjusting the Nrf2/Keap1 signaling pathway. This finding provides valuable insights into the mechanisms governing oocyte maturation and embryonic development.
doi_str_mv 10.1371/journal.pone.0311819
format article
fullrecord <record><control><sourceid>gale_plos_</sourceid><recordid>TN_cdi_plos_journals_3115393887</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A811834062</galeid><sourcerecordid>A811834062</sourcerecordid><originalsourceid>FETCH-LOGICAL-c506t-b1d565e355f66d059bb0415747ab04492b0b6f6742cb45e41c0ec0e1935e96603</originalsourceid><addsrcrecordid>eNqNkltv1DAQhSMEoqXwDxBYQkLwsFs7vuzmCVUVl4qKSlB4tRxnkrhK7NR2oPvvcbpptYv6gBLJVvKdGfvMybKXBC8JXZHjKzd6q7rl4CwsMSVkTYpH2SEpaL4QOaaPd_YH2bMQrjDmdC3E0-yAFnS9ZowfZteXLSBlo3E3pkorKiGOnbFGI6VNhcC2ymoIaHBeGwvIOb2JgHoVR6-SzKLYejc2Lfrm6_z4K6iBoGCadDRjGzSo2P5RG9S7auxu-efZk1p1AV7M61H289PHy9Mvi_OLz2enJ-cLzbGIi5JUXHCgnNdCVJgXZYkZ4Su2UmnDirzEpajFiuW6ZBwY0RjSm67MoRAC06Ps9bbu0LkgZ7eCTEbx2-uvEvFhJsayh0qDjV51cvCmV34jnTJy_481rWzcb0kIE4LlU493cwXvrkcIUfYmaOg6ZcGN22YcJ98n9M0_6MNHmqlGdSCNrV1qrKei8mSdRkwZFnmilg9Q6amgNzrloTbp-57g_Z4gMRFuYqPGEOTZj-__z1782mff7rAtqC62wXXjNOewD7ItqL0LwUN97zLBcorznRtyirOc45xkr3YndC-6yy_9C8LE8GQ</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3115393887</pqid></control><display><type>article</type><title>The antioxidant betulinic acid enhances porcine oocyte maturation through Nrf2/Keap1 signaling pathway modulation</title><source>PubMed Central Free</source><source>Publicly Available Content (ProQuest)</source><creator>Kim, Min Ju ; Kang, Hyo-Gu ; Jeon, Se-Been ; Yun, Ji Hyeon ; Jeong, Pil-Soo ; Sim, Bo-Woong ; Kim, Sun-Uk ; Cho, Seong-Keun ; Song, Bong-Seok</creator><contributor>Zhang, Meijia</contributor><creatorcontrib>Kim, Min Ju ; Kang, Hyo-Gu ; Jeon, Se-Been ; Yun, Ji Hyeon ; Jeong, Pil-Soo ; Sim, Bo-Woong ; Kim, Sun-Uk ; Cho, Seong-Keun ; Song, Bong-Seok ; Zhang, Meijia</creatorcontrib><description>During in vitro maturation, excess levels of reactive oxygen species (ROS) are a major cause of developmental defects in embryos. Betulinic acid (BA) is a naturally produced antioxidant in white birch bark. Recent studies have shown that BA exhibits antioxidant properties in various cells through the activation of antioxidant genes. Therefore, we investigated the effect of BA treatment on porcine oocytes and its underlying mechanism during oocyte maturation. Treatment with 0.1 μM BA significantly increased the proportion of MII oocytes compared with controls, and BA-treated oocytes had significantly higher development rates, trophectoderm cell numbers, and cell survival rates than controls. These results demonstrate that BA treatment improved the developmental competence of oocytes. Following BA treatment, oocytes exhibited reduced ROS levels and elevated glutathione (GSH) levels, accompanied by the enhanced expression of antioxidant genes, compared with control oocytes. To evaluate the antioxidant effects of BA, oocytes were exposed to H2O2, a potent ROS activator. Impaired nuclear maturation, ROS levels, and GSH levels induced in oocytes by H2O2 exposure was restored by BA treatment. As these antioxidant genes are regulated by the Nrf2/Keap1 signaling pathway, which is involved in antioxidant responses, we applied the Nrf2 inhibitor brusatol to investigate the effects of BA on this pathway. The negative effects of brusatol on meiotic maturation and oocyte quality, including levels of ROS, GSH, and antioxidant-related gene expression, were mitigated by BA treatment. Our results suggested that BA plays an effective role as an antioxidant in porcine oocyte maturation through adjusting the Nrf2/Keap1 signaling pathway. This finding provides valuable insights into the mechanisms governing oocyte maturation and embryonic development.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0311819</identifier><identifier>PMID: 39388445</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Antioxidants ; Antioxidants - pharmacology ; Apoptosis ; Bark ; Betulinic Acid ; Biology and Life Sciences ; Cell activation ; Cell survival ; Chemicals ; Defense mechanisms ; Embryogenesis ; Embryonic development ; Embryonic growth stage ; Embryos ; Evaluation ; Female ; Gametocytes ; Gene expression ; Genes ; Glutathione ; Glutathione - metabolism ; Growth ; Health aspects ; Hydrogen Peroxide ; Kelch-Like ECH-Associated Protein 1 - genetics ; Kelch-Like ECH-Associated Protein 1 - metabolism ; Laboratories ; Maturation ; Medicine and Health Sciences ; Meiosis ; NF-E2-Related Factor 2 - genetics ; NF-E2-Related Factor 2 - metabolism ; NRF2 protein ; Oocytes ; Oocytes - drug effects ; Oocytes - metabolism ; Ovaries ; Oxidative stress ; Pentacyclic Triterpenes ; Physiology ; Reactive oxygen species ; Reactive Oxygen Species - metabolism ; Signal transduction ; Signal Transduction - drug effects ; Survival ; Swine ; Transcription activation ; Triterpenes - pharmacology ; Trophectoderm</subject><ispartof>PloS one, 2024-10, Vol.19 (10), p.e0311819</ispartof><rights>Copyright: © 2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Kim et al 2024 Kim et al</rights><rights>2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c506t-b1d565e355f66d059bb0415747ab04492b0b6f6742cb45e41c0ec0e1935e96603</cites><orcidid>0000-0002-0489-6719 ; 0000-0002-8329-1709</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3115393887/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3115393887?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39388445$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Zhang, Meijia</contributor><creatorcontrib>Kim, Min Ju</creatorcontrib><creatorcontrib>Kang, Hyo-Gu</creatorcontrib><creatorcontrib>Jeon, Se-Been</creatorcontrib><creatorcontrib>Yun, Ji Hyeon</creatorcontrib><creatorcontrib>Jeong, Pil-Soo</creatorcontrib><creatorcontrib>Sim, Bo-Woong</creatorcontrib><creatorcontrib>Kim, Sun-Uk</creatorcontrib><creatorcontrib>Cho, Seong-Keun</creatorcontrib><creatorcontrib>Song, Bong-Seok</creatorcontrib><title>The antioxidant betulinic acid enhances porcine oocyte maturation through Nrf2/Keap1 signaling pathway modulation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>During in vitro maturation, excess levels of reactive oxygen species (ROS) are a major cause of developmental defects in embryos. Betulinic acid (BA) is a naturally produced antioxidant in white birch bark. Recent studies have shown that BA exhibits antioxidant properties in various cells through the activation of antioxidant genes. Therefore, we investigated the effect of BA treatment on porcine oocytes and its underlying mechanism during oocyte maturation. Treatment with 0.1 μM BA significantly increased the proportion of MII oocytes compared with controls, and BA-treated oocytes had significantly higher development rates, trophectoderm cell numbers, and cell survival rates than controls. These results demonstrate that BA treatment improved the developmental competence of oocytes. Following BA treatment, oocytes exhibited reduced ROS levels and elevated glutathione (GSH) levels, accompanied by the enhanced expression of antioxidant genes, compared with control oocytes. To evaluate the antioxidant effects of BA, oocytes were exposed to H2O2, a potent ROS activator. Impaired nuclear maturation, ROS levels, and GSH levels induced in oocytes by H2O2 exposure was restored by BA treatment. As these antioxidant genes are regulated by the Nrf2/Keap1 signaling pathway, which is involved in antioxidant responses, we applied the Nrf2 inhibitor brusatol to investigate the effects of BA on this pathway. The negative effects of brusatol on meiotic maturation and oocyte quality, including levels of ROS, GSH, and antioxidant-related gene expression, were mitigated by BA treatment. Our results suggested that BA plays an effective role as an antioxidant in porcine oocyte maturation through adjusting the Nrf2/Keap1 signaling pathway. This finding provides valuable insights into the mechanisms governing oocyte maturation and embryonic development.</description><subject>Animals</subject><subject>Antioxidants</subject><subject>Antioxidants - pharmacology</subject><subject>Apoptosis</subject><subject>Bark</subject><subject>Betulinic Acid</subject><subject>Biology and Life Sciences</subject><subject>Cell activation</subject><subject>Cell survival</subject><subject>Chemicals</subject><subject>Defense mechanisms</subject><subject>Embryogenesis</subject><subject>Embryonic development</subject><subject>Embryonic growth stage</subject><subject>Embryos</subject><subject>Evaluation</subject><subject>Female</subject><subject>Gametocytes</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Glutathione</subject><subject>Glutathione - metabolism</subject><subject>Growth</subject><subject>Health aspects</subject><subject>Hydrogen Peroxide</subject><subject>Kelch-Like ECH-Associated Protein 1 - genetics</subject><subject>Kelch-Like ECH-Associated Protein 1 - metabolism</subject><subject>Laboratories</subject><subject>Maturation</subject><subject>Medicine and Health Sciences</subject><subject>Meiosis</subject><subject>NF-E2-Related Factor 2 - genetics</subject><subject>NF-E2-Related Factor 2 - metabolism</subject><subject>NRF2 protein</subject><subject>Oocytes</subject><subject>Oocytes - drug effects</subject><subject>Oocytes - metabolism</subject><subject>Ovaries</subject><subject>Oxidative stress</subject><subject>Pentacyclic Triterpenes</subject><subject>Physiology</subject><subject>Reactive oxygen species</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Survival</subject><subject>Swine</subject><subject>Transcription activation</subject><subject>Triterpenes - pharmacology</subject><subject>Trophectoderm</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNqNkltv1DAQhSMEoqXwDxBYQkLwsFs7vuzmCVUVl4qKSlB4tRxnkrhK7NR2oPvvcbpptYv6gBLJVvKdGfvMybKXBC8JXZHjKzd6q7rl4CwsMSVkTYpH2SEpaL4QOaaPd_YH2bMQrjDmdC3E0-yAFnS9ZowfZteXLSBlo3E3pkorKiGOnbFGI6VNhcC2ymoIaHBeGwvIOb2JgHoVR6-SzKLYejc2Lfrm6_z4K6iBoGCadDRjGzSo2P5RG9S7auxu-efZk1p1AV7M61H289PHy9Mvi_OLz2enJ-cLzbGIi5JUXHCgnNdCVJgXZYkZ4Su2UmnDirzEpajFiuW6ZBwY0RjSm67MoRAC06Ps9bbu0LkgZ7eCTEbx2-uvEvFhJsayh0qDjV51cvCmV34jnTJy_481rWzcb0kIE4LlU493cwXvrkcIUfYmaOg6ZcGN22YcJ98n9M0_6MNHmqlGdSCNrV1qrKei8mSdRkwZFnmilg9Q6amgNzrloTbp-57g_Z4gMRFuYqPGEOTZj-__z1782mff7rAtqC62wXXjNOewD7ItqL0LwUN97zLBcorznRtyirOc45xkr3YndC-6yy_9C8LE8GQ</recordid><startdate>20241010</startdate><enddate>20241010</enddate><creator>Kim, Min Ju</creator><creator>Kang, Hyo-Gu</creator><creator>Jeon, Se-Been</creator><creator>Yun, Ji Hyeon</creator><creator>Jeong, Pil-Soo</creator><creator>Sim, Bo-Woong</creator><creator>Kim, Sun-Uk</creator><creator>Cho, Seong-Keun</creator><creator>Song, Bong-Seok</creator><general>Public Library of Science</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0489-6719</orcidid><orcidid>https://orcid.org/0000-0002-8329-1709</orcidid></search><sort><creationdate>20241010</creationdate><title>The antioxidant betulinic acid enhances porcine oocyte maturation through Nrf2/Keap1 signaling pathway modulation</title><author>Kim, Min Ju ; Kang, Hyo-Gu ; Jeon, Se-Been ; Yun, Ji Hyeon ; Jeong, Pil-Soo ; Sim, Bo-Woong ; Kim, Sun-Uk ; Cho, Seong-Keun ; Song, Bong-Seok</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c506t-b1d565e355f66d059bb0415747ab04492b0b6f6742cb45e41c0ec0e1935e96603</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Antioxidants</topic><topic>Antioxidants - pharmacology</topic><topic>Apoptosis</topic><topic>Bark</topic><topic>Betulinic Acid</topic><topic>Biology and Life Sciences</topic><topic>Cell activation</topic><topic>Cell survival</topic><topic>Chemicals</topic><topic>Defense mechanisms</topic><topic>Embryogenesis</topic><topic>Embryonic development</topic><topic>Embryonic growth stage</topic><topic>Embryos</topic><topic>Evaluation</topic><topic>Female</topic><topic>Gametocytes</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Glutathione</topic><topic>Glutathione - metabolism</topic><topic>Growth</topic><topic>Health aspects</topic><topic>Hydrogen Peroxide</topic><topic>Kelch-Like ECH-Associated Protein 1 - genetics</topic><topic>Kelch-Like ECH-Associated Protein 1 - metabolism</topic><topic>Laboratories</topic><topic>Maturation</topic><topic>Medicine and Health Sciences</topic><topic>Meiosis</topic><topic>NF-E2-Related Factor 2 - genetics</topic><topic>NF-E2-Related Factor 2 - metabolism</topic><topic>NRF2 protein</topic><topic>Oocytes</topic><topic>Oocytes - drug effects</topic><topic>Oocytes - metabolism</topic><topic>Ovaries</topic><topic>Oxidative stress</topic><topic>Pentacyclic Triterpenes</topic><topic>Physiology</topic><topic>Reactive oxygen species</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>Signal transduction</topic><topic>Signal Transduction - drug effects</topic><topic>Survival</topic><topic>Swine</topic><topic>Transcription activation</topic><topic>Triterpenes - pharmacology</topic><topic>Trophectoderm</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Min Ju</creatorcontrib><creatorcontrib>Kang, Hyo-Gu</creatorcontrib><creatorcontrib>Jeon, Se-Been</creatorcontrib><creatorcontrib>Yun, Ji Hyeon</creatorcontrib><creatorcontrib>Jeong, Pil-Soo</creatorcontrib><creatorcontrib>Sim, Bo-Woong</creatorcontrib><creatorcontrib>Kim, Sun-Uk</creatorcontrib><creatorcontrib>Cho, Seong-Keun</creatorcontrib><creatorcontrib>Song, Bong-Seok</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Opposing Viewpoints Resource Center</collection><collection>Science (Gale in Context)</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; Allied Health Database (ProQuest)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest - Health &amp; Medical Complete保健、医学与药学数据库</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database (Proquest)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>ProQuest Biological Science Journals</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>ProQuest advanced technologies &amp; aerospace journals</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials science collection</collection><collection>Publicly Available Content (ProQuest)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kim, Min Ju</au><au>Kang, Hyo-Gu</au><au>Jeon, Se-Been</au><au>Yun, Ji Hyeon</au><au>Jeong, Pil-Soo</au><au>Sim, Bo-Woong</au><au>Kim, Sun-Uk</au><au>Cho, Seong-Keun</au><au>Song, Bong-Seok</au><au>Zhang, Meijia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The antioxidant betulinic acid enhances porcine oocyte maturation through Nrf2/Keap1 signaling pathway modulation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2024-10-10</date><risdate>2024</risdate><volume>19</volume><issue>10</issue><spage>e0311819</spage><pages>e0311819-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>During in vitro maturation, excess levels of reactive oxygen species (ROS) are a major cause of developmental defects in embryos. Betulinic acid (BA) is a naturally produced antioxidant in white birch bark. Recent studies have shown that BA exhibits antioxidant properties in various cells through the activation of antioxidant genes. Therefore, we investigated the effect of BA treatment on porcine oocytes and its underlying mechanism during oocyte maturation. Treatment with 0.1 μM BA significantly increased the proportion of MII oocytes compared with controls, and BA-treated oocytes had significantly higher development rates, trophectoderm cell numbers, and cell survival rates than controls. These results demonstrate that BA treatment improved the developmental competence of oocytes. Following BA treatment, oocytes exhibited reduced ROS levels and elevated glutathione (GSH) levels, accompanied by the enhanced expression of antioxidant genes, compared with control oocytes. To evaluate the antioxidant effects of BA, oocytes were exposed to H2O2, a potent ROS activator. Impaired nuclear maturation, ROS levels, and GSH levels induced in oocytes by H2O2 exposure was restored by BA treatment. As these antioxidant genes are regulated by the Nrf2/Keap1 signaling pathway, which is involved in antioxidant responses, we applied the Nrf2 inhibitor brusatol to investigate the effects of BA on this pathway. The negative effects of brusatol on meiotic maturation and oocyte quality, including levels of ROS, GSH, and antioxidant-related gene expression, were mitigated by BA treatment. Our results suggested that BA plays an effective role as an antioxidant in porcine oocyte maturation through adjusting the Nrf2/Keap1 signaling pathway. This finding provides valuable insights into the mechanisms governing oocyte maturation and embryonic development.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39388445</pmid><doi>10.1371/journal.pone.0311819</doi><tpages>e0311819</tpages><orcidid>https://orcid.org/0000-0002-0489-6719</orcidid><orcidid>https://orcid.org/0000-0002-8329-1709</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1932-6203
ispartof PloS one, 2024-10, Vol.19 (10), p.e0311819
issn 1932-6203
1932-6203
language eng
recordid cdi_plos_journals_3115393887
source PubMed Central Free; Publicly Available Content (ProQuest)
subjects Animals
Antioxidants
Antioxidants - pharmacology
Apoptosis
Bark
Betulinic Acid
Biology and Life Sciences
Cell activation
Cell survival
Chemicals
Defense mechanisms
Embryogenesis
Embryonic development
Embryonic growth stage
Embryos
Evaluation
Female
Gametocytes
Gene expression
Genes
Glutathione
Glutathione - metabolism
Growth
Health aspects
Hydrogen Peroxide
Kelch-Like ECH-Associated Protein 1 - genetics
Kelch-Like ECH-Associated Protein 1 - metabolism
Laboratories
Maturation
Medicine and Health Sciences
Meiosis
NF-E2-Related Factor 2 - genetics
NF-E2-Related Factor 2 - metabolism
NRF2 protein
Oocytes
Oocytes - drug effects
Oocytes - metabolism
Ovaries
Oxidative stress
Pentacyclic Triterpenes
Physiology
Reactive oxygen species
Reactive Oxygen Species - metabolism
Signal transduction
Signal Transduction - drug effects
Survival
Swine
Transcription activation
Triterpenes - pharmacology
Trophectoderm
title The antioxidant betulinic acid enhances porcine oocyte maturation through Nrf2/Keap1 signaling pathway modulation
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-21T14%3A38%3A45IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20antioxidant%20betulinic%20acid%20enhances%20porcine%20oocyte%20maturation%20through%20Nrf2/Keap1%20signaling%20pathway%20modulation&rft.jtitle=PloS%20one&rft.au=Kim,%20Min%20Ju&rft.date=2024-10-10&rft.volume=19&rft.issue=10&rft.spage=e0311819&rft.pages=e0311819-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0311819&rft_dat=%3Cgale_plos_%3EA811834062%3C/gale_plos_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c506t-b1d565e355f66d059bb0415747ab04492b0b6f6742cb45e41c0ec0e1935e96603%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=3115393887&rft_id=info:pmid/39388445&rft_galeid=A811834062&rfr_iscdi=true