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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...
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Published in: | PloS one 2024-10, Vol.19 (10), p.e0311819 |
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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. |
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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 - 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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> |
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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 |
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