Butylparaben Is Toxic to Porcine Oocyte Maturation and Subsequent Embryonic Development Following In Vitro Fertilization
Parabens are widely used in personal care products due to their antimicrobial effects. Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of B...
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creator | Jeong, Pil-Soo Lee, Sanghoon Park, Soo-Hyun Kim, Min Ju Kang, Hyo-Gu Nanjidsuren, Tsevelmaa Son, Hee-Chang Song, Bong-Seok Koo, Deog-Bon Sim, Bo-Woong Kim, Sun-Uk |
description | Parabens are widely used in personal care products due to their antimicrobial effects. Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of BP (0 μM, 100 μM, 200 μM, 300 μM, 400 μM, and 500 μM) on the in vitro maturation of porcine oocytes. BP supplementation at a concentration greater than 300 μM significantly reduced the proportion of complete cumulus cell expansion and metaphase II oocytes compared to the control. The 300 μM BP significantly decreased fertilization, cleavage, and blastocyst formation rates with lower total cell numbers and a higher rate of apoptosis in blastocysts compared to the control. The BP-treated oocytes showed significantly higher reactive oxygen species (ROS) levels, and lower glutathione (GSH) levels than the control. BP significantly increased the aberrant mitochondrial distribution and decreased mitochondrial function compared to the control. BP-treated oocytes exhibited significantly higher percentage of γ-H2AX, annexin V-positive oocytes and expression of LC3 than the control. In conclusion, we demonstrated that BP impaired oocyte maturation and subsequent embryonic development, by inducing ROS generation and reducing GSH levels. Furthermore, BP disrupted mitochondrial function and triggered DNA damage, early apoptosis, and autophagy in oocytes. |
doi_str_mv | 10.3390/ijms21103692 |
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Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of BP (0 μM, 100 μM, 200 μM, 300 μM, 400 μM, and 500 μM) on the in vitro maturation of porcine oocytes. BP supplementation at a concentration greater than 300 μM significantly reduced the proportion of complete cumulus cell expansion and metaphase II oocytes compared to the control. The 300 μM BP significantly decreased fertilization, cleavage, and blastocyst formation rates with lower total cell numbers and a higher rate of apoptosis in blastocysts compared to the control. The BP-treated oocytes showed significantly higher reactive oxygen species (ROS) levels, and lower glutathione (GSH) levels than the control. BP significantly increased the aberrant mitochondrial distribution and decreased mitochondrial function compared to the control. BP-treated oocytes exhibited significantly higher percentage of γ-H2AX, annexin V-positive oocytes and expression of LC3 than the control. In conclusion, we demonstrated that BP impaired oocyte maturation and subsequent embryonic development, by inducing ROS generation and reducing GSH levels. Furthermore, BP disrupted mitochondrial function and triggered DNA damage, early apoptosis, and autophagy in oocytes.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms21103692</identifier><identifier>PMID: 32456265</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Animals ; Annexin V ; Apoptosis ; Autophagy ; Blastocyst - drug effects ; Blastocyst - metabolism ; Blastocysts ; Cosmetics ; Deoxyribonucleic acid ; DNA ; DNA damage ; Embryogenesis ; Embryonic Development - drug effects ; Embryos ; Fertilization in Vitro - drug effects ; Gametocytes ; Glutathione ; In vitro fertilization ; Maturation ; Metaphase ; Mitochondria ; Mitochondrial DNA ; Oocytes ; Oocytes - drug effects ; Oogenesis - drug effects ; Parabens - adverse effects ; Parabens - toxicity ; Personal grooming ; Phagocytosis ; Physiology ; Reactive Oxygen Species ; Reproductive system ; Surface water ; Sus scrofa - embryology ; Sus scrofa - physiology ; Toxicity</subject><ispartof>International journal of molecular sciences, 2020-05, Vol.21 (10), p.3692</ispartof><rights>2020. This work is licensed under http://creativecommons.org/licenses/by/3.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2020 by the authors. 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-bfb26ae13a9f707ebefe9801a754d59a705f01367a3dac4e9c25c6287d8a4f1d3</citedby><cites>FETCH-LOGICAL-c412t-bfb26ae13a9f707ebefe9801a754d59a705f01367a3dac4e9c25c6287d8a4f1d3</cites><orcidid>0000-0002-4492-1085 ; 0000-0001-7825-9598</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7279239/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7279239/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32456265$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jeong, Pil-Soo</creatorcontrib><creatorcontrib>Lee, Sanghoon</creatorcontrib><creatorcontrib>Park, Soo-Hyun</creatorcontrib><creatorcontrib>Kim, Min Ju</creatorcontrib><creatorcontrib>Kang, Hyo-Gu</creatorcontrib><creatorcontrib>Nanjidsuren, Tsevelmaa</creatorcontrib><creatorcontrib>Son, Hee-Chang</creatorcontrib><creatorcontrib>Song, Bong-Seok</creatorcontrib><creatorcontrib>Koo, Deog-Bon</creatorcontrib><creatorcontrib>Sim, Bo-Woong</creatorcontrib><creatorcontrib>Kim, Sun-Uk</creatorcontrib><title>Butylparaben Is Toxic to Porcine Oocyte Maturation and Subsequent Embryonic Development Following In Vitro Fertilization</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Parabens are widely used in personal care products due to their antimicrobial effects. Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of BP (0 μM, 100 μM, 200 μM, 300 μM, 400 μM, and 500 μM) on the in vitro maturation of porcine oocytes. BP supplementation at a concentration greater than 300 μM significantly reduced the proportion of complete cumulus cell expansion and metaphase II oocytes compared to the control. The 300 μM BP significantly decreased fertilization, cleavage, and blastocyst formation rates with lower total cell numbers and a higher rate of apoptosis in blastocysts compared to the control. The BP-treated oocytes showed significantly higher reactive oxygen species (ROS) levels, and lower glutathione (GSH) levels than the control. BP significantly increased the aberrant mitochondrial distribution and decreased mitochondrial function compared to the control. BP-treated oocytes exhibited significantly higher percentage of γ-H2AX, annexin V-positive oocytes and expression of LC3 than the control. In conclusion, we demonstrated that BP impaired oocyte maturation and subsequent embryonic development, by inducing ROS generation and reducing GSH levels. Furthermore, BP disrupted mitochondrial function and triggered DNA damage, early apoptosis, and autophagy in oocytes.</description><subject>Animals</subject><subject>Annexin V</subject><subject>Apoptosis</subject><subject>Autophagy</subject><subject>Blastocyst - drug effects</subject><subject>Blastocyst - metabolism</subject><subject>Blastocysts</subject><subject>Cosmetics</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA damage</subject><subject>Embryogenesis</subject><subject>Embryonic Development - drug effects</subject><subject>Embryos</subject><subject>Fertilization in Vitro - drug effects</subject><subject>Gametocytes</subject><subject>Glutathione</subject><subject>In vitro fertilization</subject><subject>Maturation</subject><subject>Metaphase</subject><subject>Mitochondria</subject><subject>Mitochondrial DNA</subject><subject>Oocytes</subject><subject>Oocytes - drug effects</subject><subject>Oogenesis - drug effects</subject><subject>Parabens - adverse effects</subject><subject>Parabens - toxicity</subject><subject>Personal grooming</subject><subject>Phagocytosis</subject><subject>Physiology</subject><subject>Reactive Oxygen Species</subject><subject>Reproductive system</subject><subject>Surface water</subject><subject>Sus scrofa - embryology</subject><subject>Sus scrofa - physiology</subject><subject>Toxicity</subject><issn>1422-0067</issn><issn>1661-6596</issn><issn>1422-0067</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>BENPR</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNpVkc1LAzEQxYMo1q-bZwl4tZqP3U1zEbS2WqgoWL2GbDZbU3aTmmSr9a93a1XqKUPmzW_e8AA4xuicUo4uzKwOBGNEM062wB5OCOkilLHtjboD9kOYIUQoSfku6FCSpBnJ0j3wcd3EZTWXXubawlGAE_dhFIwOPjqvjNXwwall1PBexsbLaJyF0hbwqcmDfmu0jXBQ537pbDt1oxe6cvN69Tt0VeXejZ3CkYUvJnoHh9pHU5nPb8oh2CllFfTRz3sAnoeDSf-uO364HfWvxl2VYBK7eZmTTGpMJS8ZYjrXpeY9hCVLkyLlkqG0RJhmTNJCqkRzRVKVkR4rejIpcUEPwOWaO2_yWheq9eZlJebe1NIvhZNG_O9Y8yqmbiEYYZxQ3gJOfwDetQeHKGau8bb1LEiCWMYQSXqt6mytUt6F4HX5twEjscpJbObUyk82Xf2Jf4OhX7mLkiE</recordid><startdate>20200524</startdate><enddate>20200524</enddate><creator>Jeong, Pil-Soo</creator><creator>Lee, Sanghoon</creator><creator>Park, Soo-Hyun</creator><creator>Kim, Min Ju</creator><creator>Kang, Hyo-Gu</creator><creator>Nanjidsuren, Tsevelmaa</creator><creator>Son, Hee-Chang</creator><creator>Song, Bong-Seok</creator><creator>Koo, Deog-Bon</creator><creator>Sim, Bo-Woong</creator><creator>Kim, Sun-Uk</creator><general>MDPI AG</general><general>MDPI</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4492-1085</orcidid><orcidid>https://orcid.org/0000-0001-7825-9598</orcidid></search><sort><creationdate>20200524</creationdate><title>Butylparaben Is Toxic to Porcine Oocyte Maturation and Subsequent Embryonic Development Following In Vitro Fertilization</title><author>Jeong, Pil-Soo ; Lee, Sanghoon ; Park, Soo-Hyun ; Kim, Min Ju ; Kang, Hyo-Gu ; Nanjidsuren, Tsevelmaa ; Son, Hee-Chang ; Song, Bong-Seok ; Koo, Deog-Bon ; Sim, Bo-Woong ; Kim, Sun-Uk</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-bfb26ae13a9f707ebefe9801a754d59a705f01367a3dac4e9c25c6287d8a4f1d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Annexin V</topic><topic>Apoptosis</topic><topic>Autophagy</topic><topic>Blastocyst - drug effects</topic><topic>Blastocyst - metabolism</topic><topic>Blastocysts</topic><topic>Cosmetics</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA damage</topic><topic>Embryogenesis</topic><topic>Embryonic Development - drug effects</topic><topic>Embryos</topic><topic>Fertilization in Vitro - drug effects</topic><topic>Gametocytes</topic><topic>Glutathione</topic><topic>In vitro fertilization</topic><topic>Maturation</topic><topic>Metaphase</topic><topic>Mitochondria</topic><topic>Mitochondrial DNA</topic><topic>Oocytes</topic><topic>Oocytes - drug effects</topic><topic>Oogenesis - drug effects</topic><topic>Parabens - adverse effects</topic><topic>Parabens - toxicity</topic><topic>Personal grooming</topic><topic>Phagocytosis</topic><topic>Physiology</topic><topic>Reactive Oxygen Species</topic><topic>Reproductive system</topic><topic>Surface water</topic><topic>Sus scrofa - embryology</topic><topic>Sus scrofa - physiology</topic><topic>Toxicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jeong, Pil-Soo</creatorcontrib><creatorcontrib>Lee, Sanghoon</creatorcontrib><creatorcontrib>Park, Soo-Hyun</creatorcontrib><creatorcontrib>Kim, Min Ju</creatorcontrib><creatorcontrib>Kang, Hyo-Gu</creatorcontrib><creatorcontrib>Nanjidsuren, Tsevelmaa</creatorcontrib><creatorcontrib>Son, Hee-Chang</creatorcontrib><creatorcontrib>Song, Bong-Seok</creatorcontrib><creatorcontrib>Koo, Deog-Bon</creatorcontrib><creatorcontrib>Sim, Bo-Woong</creatorcontrib><creatorcontrib>Kim, Sun-Uk</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Research Library (Corporate)</collection><collection>Publicly Available Content Database</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>ProQuest Central Basic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of molecular sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jeong, Pil-Soo</au><au>Lee, Sanghoon</au><au>Park, Soo-Hyun</au><au>Kim, Min Ju</au><au>Kang, Hyo-Gu</au><au>Nanjidsuren, Tsevelmaa</au><au>Son, Hee-Chang</au><au>Song, Bong-Seok</au><au>Koo, Deog-Bon</au><au>Sim, Bo-Woong</au><au>Kim, Sun-Uk</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Butylparaben Is Toxic to Porcine Oocyte Maturation and Subsequent Embryonic Development Following In Vitro Fertilization</atitle><jtitle>International journal of molecular sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2020-05-24</date><risdate>2020</risdate><volume>21</volume><issue>10</issue><spage>3692</spage><pages>3692-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Parabens are widely used in personal care products due to their antimicrobial effects. Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of BP (0 μM, 100 μM, 200 μM, 300 μM, 400 μM, and 500 μM) on the in vitro maturation of porcine oocytes. BP supplementation at a concentration greater than 300 μM significantly reduced the proportion of complete cumulus cell expansion and metaphase II oocytes compared to the control. The 300 μM BP significantly decreased fertilization, cleavage, and blastocyst formation rates with lower total cell numbers and a higher rate of apoptosis in blastocysts compared to the control. The BP-treated oocytes showed significantly higher reactive oxygen species (ROS) levels, and lower glutathione (GSH) levels than the control. BP significantly increased the aberrant mitochondrial distribution and decreased mitochondrial function compared to the control. BP-treated oocytes exhibited significantly higher percentage of γ-H2AX, annexin V-positive oocytes and expression of LC3 than the control. In conclusion, we demonstrated that BP impaired oocyte maturation and subsequent embryonic development, by inducing ROS generation and reducing GSH levels. Furthermore, BP disrupted mitochondrial function and triggered DNA damage, early apoptosis, and autophagy in oocytes.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>32456265</pmid><doi>10.3390/ijms21103692</doi><orcidid>https://orcid.org/0000-0002-4492-1085</orcidid><orcidid>https://orcid.org/0000-0001-7825-9598</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Annexin V Apoptosis Autophagy Blastocyst - drug effects Blastocyst - metabolism Blastocysts Cosmetics Deoxyribonucleic acid DNA DNA damage Embryogenesis Embryonic Development - drug effects Embryos Fertilization in Vitro - drug effects Gametocytes Glutathione In vitro fertilization Maturation Metaphase Mitochondria Mitochondrial DNA Oocytes Oocytes - drug effects Oogenesis - drug effects Parabens - adverse effects Parabens - toxicity Personal grooming Phagocytosis Physiology Reactive Oxygen Species Reproductive system Surface water Sus scrofa - embryology Sus scrofa - physiology Toxicity |
title | Butylparaben Is Toxic to Porcine Oocyte Maturation and Subsequent Embryonic Development Following In Vitro Fertilization |
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