Safe concentration, unsafe effects: Impact of BPA on antioxidant function in the hepatopancreas and ovarian gene expression in oriental river prawns (Macrobrachium nipponense)

•The 24hLC50 and 48hLC50 of BPA for M. nipponense are 80.59 and 63.90 mg/L.•BPA enhances ovarian gene expression, causing precocious puberty and miniaturization.•Even safe-level BPA causes oxidative stress, affecting ovarian development.•The biological damage caused by BPA is reversible. This study...

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Veröffentlicht in:Aquatic toxicology 2024-11, Vol.276, p.107103, Article 107103
Hauptverfasser: Zhao, Weihong, Zheng, Xirui, Jiang, Fengjuan, Liu, Jintao, Wang, Shuhao, Ou, Jiangtao
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container_start_page 107103
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creator Zhao, Weihong
Zheng, Xirui
Jiang, Fengjuan
Liu, Jintao
Wang, Shuhao
Ou, Jiangtao
description •The 24hLC50 and 48hLC50 of BPA for M. nipponense are 80.59 and 63.90 mg/L.•BPA enhances ovarian gene expression, causing precocious puberty and miniaturization.•Even safe-level BPA causes oxidative stress, affecting ovarian development.•The biological damage caused by BPA is reversible. This study investigated the effects of Bisphenol A (BPA), a common endocrine-disrupting chemical, on the antioxidant enzyme activities in the hepatopancreas and the expression of genes related to ovarian development in oriental river prawns (Macrobrachium nipponense). The 24hLC50 and 48hLC50 values for BPA were 80.59 mg/L and 63.90 mg/L, respectively, with a safe concentration of 12.06 mg/L. Prawns were exposed to low (4.85 mg/L), safe (12.06 mg/L), and high (30.00 mg/L) concentrations of BPA for 10 days to measure enzyme activities, and for 20 days followed by 7 days in BPA-free water to measure gene expression. Short-term exposure (12 h, 1d, 3d) to low concentration BPA did not significantly affect superoxide dismutase (SOD) activity in the hepatopancreas (P > 0.05), but long-term exposure (6d, 10d) significantly reduced SOD activity (P < 0.05). Catalase (CAT) activity showed no significant changes throughout the low concentration exposure period (P > 0.05). At safe and high concentrations, SOD and CAT activities significantly decreased after 12 h of exposure (P < 0.05). BPA affected heat shock protein 90 (HSP90) expression in the ovary, with low concentration BPA significantly upregulating HSP90 after 1 day (P < 0.05), but returning to normal levels after 10 and 20 days. At the safe concentration, HSP90 was significantly upregulated at all three sampling points (1d, 10d, 20d) (P < 0.05), while high concentration exposure led to significant upregulation only on day 10 (P < 0.05). Low concentration BPA had no significant effect on Cathepsin B (CB) and Cathepsin L (CL) gene expression in the ovaries (P > 0.05). However, safe concentration exposure promoted CB expression on days 1, 10, and 20 (P < 0.05), while high concentration exposure significantly increased CB expression on day 1 (P < 0.05), with levels returning to normal on days 10 and 20. CL expression significantly increased after 20 days of exposure to both safe and high concentrations (P < 0.05). Gene expression levels in the ovaries returned to normal after transfer to BPA-free water, with HSP90 and CB normalizing by day 1, and CL by day 7. These results indicate that even safe concentrations of BPA impose stress
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This study investigated the effects of Bisphenol A (BPA), a common endocrine-disrupting chemical, on the antioxidant enzyme activities in the hepatopancreas and the expression of genes related to ovarian development in oriental river prawns (Macrobrachium nipponense). The 24hLC50 and 48hLC50 values for BPA were 80.59 mg/L and 63.90 mg/L, respectively, with a safe concentration of 12.06 mg/L. Prawns were exposed to low (4.85 mg/L), safe (12.06 mg/L), and high (30.00 mg/L) concentrations of BPA for 10 days to measure enzyme activities, and for 20 days followed by 7 days in BPA-free water to measure gene expression. Short-term exposure (12 h, 1d, 3d) to low concentration BPA did not significantly affect superoxide dismutase (SOD) activity in the hepatopancreas (P > 0.05), but long-term exposure (6d, 10d) significantly reduced SOD activity (P < 0.05). Catalase (CAT) activity showed no significant changes throughout the low concentration exposure period (P > 0.05). At safe and high concentrations, SOD and CAT activities significantly decreased after 12 h of exposure (P < 0.05). BPA affected heat shock protein 90 (HSP90) expression in the ovary, with low concentration BPA significantly upregulating HSP90 after 1 day (P < 0.05), but returning to normal levels after 10 and 20 days. At the safe concentration, HSP90 was significantly upregulated at all three sampling points (1d, 10d, 20d) (P < 0.05), while high concentration exposure led to significant upregulation only on day 10 (P < 0.05). Low concentration BPA had no significant effect on Cathepsin B (CB) and Cathepsin L (CL) gene expression in the ovaries (P > 0.05). However, safe concentration exposure promoted CB expression on days 1, 10, and 20 (P < 0.05), while high concentration exposure significantly increased CB expression on day 1 (P < 0.05), with levels returning to normal on days 10 and 20. CL expression significantly increased after 20 days of exposure to both safe and high concentrations (P < 0.05). Gene expression levels in the ovaries returned to normal after transfer to BPA-free water, with HSP90 and CB normalizing by day 1, and CL by day 7. These results indicate that even safe concentrations of BPA impose stress on the hepatopancreas and increase the expression of HSP90, CB, and CL genes in the ovaries, affecting ovarian development. And, these effects are reversible within a certain period after the removal of BPA.]]></description><identifier>ISSN: 0166-445X</identifier><identifier>ISSN: 1879-1514</identifier><identifier>EISSN: 1879-1514</identifier><identifier>DOI: 10.1016/j.aquatox.2024.107103</identifier><identifier>PMID: 39305710</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>acute exposure ; Acute lethal effect ; Animals ; antioxidant activity ; antioxidant enzymes ; Antioxidant reductase ; Antioxidants - metabolism ; Benzhydryl Compounds - toxicity ; Bisphenol A ; catalase ; Catalase - genetics ; Catalase - metabolism ; Cathepsin B ; Cathepsin L ; chronic exposure ; Endocrine Disruptors - toxicity ; endocrine-disrupting chemicals ; Female ; gene expression ; Gene Expression Regulation - drug effects ; Heat shock protein 90 ; hepatopancreas ; Hepatopancreas - drug effects ; Hepatopancreas - metabolism ; HSP90 Heat-Shock Proteins - genetics ; HSP90 Heat-Shock Proteins - metabolism ; Macrobrachium nipponense ; ovarian development ; Ovary - drug effects ; Ovary - metabolism ; Palaemonidae - drug effects ; Palaemonidae - genetics ; Phenols - toxicity ; rivers ; superoxide dismutase ; Superoxide Dismutase - genetics ; Superoxide Dismutase - metabolism ; toxicology ; Water Pollutants, Chemical - toxicity</subject><ispartof>Aquatic toxicology, 2024-11, Vol.276, p.107103, Article 107103</ispartof><rights>2024</rights><rights>Copyright © 2024. Published by Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c276t-1a01c4838cca5f8c1203fe5c857725a6485206115bd0af46e1582d8c118161243</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0166445X2400273X$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39305710$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhao, Weihong</creatorcontrib><creatorcontrib>Zheng, Xirui</creatorcontrib><creatorcontrib>Jiang, Fengjuan</creatorcontrib><creatorcontrib>Liu, Jintao</creatorcontrib><creatorcontrib>Wang, Shuhao</creatorcontrib><creatorcontrib>Ou, Jiangtao</creatorcontrib><title>Safe concentration, unsafe effects: Impact of BPA on antioxidant function in the hepatopancreas and ovarian gene expression in oriental river prawns (Macrobrachium nipponense)</title><title>Aquatic toxicology</title><addtitle>Aquat Toxicol</addtitle><description><![CDATA[•The 24hLC50 and 48hLC50 of BPA for M. nipponense are 80.59 and 63.90 mg/L.•BPA enhances ovarian gene expression, causing precocious puberty and miniaturization.•Even safe-level BPA causes oxidative stress, affecting ovarian development.•The biological damage caused by BPA is reversible. This study investigated the effects of Bisphenol A (BPA), a common endocrine-disrupting chemical, on the antioxidant enzyme activities in the hepatopancreas and the expression of genes related to ovarian development in oriental river prawns (Macrobrachium nipponense). The 24hLC50 and 48hLC50 values for BPA were 80.59 mg/L and 63.90 mg/L, respectively, with a safe concentration of 12.06 mg/L. Prawns were exposed to low (4.85 mg/L), safe (12.06 mg/L), and high (30.00 mg/L) concentrations of BPA for 10 days to measure enzyme activities, and for 20 days followed by 7 days in BPA-free water to measure gene expression. Short-term exposure (12 h, 1d, 3d) to low concentration BPA did not significantly affect superoxide dismutase (SOD) activity in the hepatopancreas (P > 0.05), but long-term exposure (6d, 10d) significantly reduced SOD activity (P < 0.05). Catalase (CAT) activity showed no significant changes throughout the low concentration exposure period (P > 0.05). At safe and high concentrations, SOD and CAT activities significantly decreased after 12 h of exposure (P < 0.05). BPA affected heat shock protein 90 (HSP90) expression in the ovary, with low concentration BPA significantly upregulating HSP90 after 1 day (P < 0.05), but returning to normal levels after 10 and 20 days. At the safe concentration, HSP90 was significantly upregulated at all three sampling points (1d, 10d, 20d) (P < 0.05), while high concentration exposure led to significant upregulation only on day 10 (P < 0.05). Low concentration BPA had no significant effect on Cathepsin B (CB) and Cathepsin L (CL) gene expression in the ovaries (P > 0.05). However, safe concentration exposure promoted CB expression on days 1, 10, and 20 (P < 0.05), while high concentration exposure significantly increased CB expression on day 1 (P < 0.05), with levels returning to normal on days 10 and 20. CL expression significantly increased after 20 days of exposure to both safe and high concentrations (P < 0.05). Gene expression levels in the ovaries returned to normal after transfer to BPA-free water, with HSP90 and CB normalizing by day 1, and CL by day 7. These results indicate that even safe concentrations of BPA impose stress on the hepatopancreas and increase the expression of HSP90, CB, and CL genes in the ovaries, affecting ovarian development. And, these effects are reversible within a certain period after the removal of BPA.]]></description><subject>acute exposure</subject><subject>Acute lethal effect</subject><subject>Animals</subject><subject>antioxidant activity</subject><subject>antioxidant enzymes</subject><subject>Antioxidant reductase</subject><subject>Antioxidants - metabolism</subject><subject>Benzhydryl Compounds - toxicity</subject><subject>Bisphenol A</subject><subject>catalase</subject><subject>Catalase - genetics</subject><subject>Catalase - metabolism</subject><subject>Cathepsin B</subject><subject>Cathepsin L</subject><subject>chronic exposure</subject><subject>Endocrine Disruptors - toxicity</subject><subject>endocrine-disrupting chemicals</subject><subject>Female</subject><subject>gene expression</subject><subject>Gene Expression Regulation - drug effects</subject><subject>Heat shock protein 90</subject><subject>hepatopancreas</subject><subject>Hepatopancreas - drug effects</subject><subject>Hepatopancreas - metabolism</subject><subject>HSP90 Heat-Shock Proteins - genetics</subject><subject>HSP90 Heat-Shock Proteins - metabolism</subject><subject>Macrobrachium nipponense</subject><subject>ovarian development</subject><subject>Ovary - drug effects</subject><subject>Ovary - metabolism</subject><subject>Palaemonidae - drug effects</subject><subject>Palaemonidae - genetics</subject><subject>Phenols - toxicity</subject><subject>rivers</subject><subject>superoxide dismutase</subject><subject>Superoxide Dismutase - genetics</subject><subject>Superoxide Dismutase - metabolism</subject><subject>toxicology</subject><subject>Water Pollutants, Chemical - toxicity</subject><issn>0166-445X</issn><issn>1879-1514</issn><issn>1879-1514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkd2O0zAQhS0EYsvCI4B8uUik2I6dpNyslhU_Ky0CCZC4s6bOmLpqbK-dlPJUvCKOWrgF34w0-s6Z8RxCnnK25Iw3L7dLuJtgDIelYEKWXstZfY8seNeuKq64vE8WhWsqKdW3M_Io5y0rT8jVQ3JWr2qmimBBfn0Gi9QEb9CPCUYX_As6-Tx30Vo0Y35Fb4YIZqTB0tefrmjwFHwBD64vldrJm1lGnafjBukGY1krgjcJIRe0p2EPyYGn39EX10NMmPNJEZIrg2FHk9tjojHBD5_pxQcwKawTmI2bBupdjMGjz_j8MXlgYZfxyamek69v33y5fl_dfnx3c311WxnRNmPFgXEju7ozBpTtDBestqhMp9pWKGhkpwRrOFfrnoGVDXLVib5wvOMNF7I-JxdH35jC3YR51IPLBnc78BimrGuupFCqsP-BsrbtpJCzqzqi5Xc5J7Q6JjdA-qk503OseqtPseo5Vn2MteienUZM6wH7v6o_ORbg8ghgucneYdLZlMMa7F0qGeo-uH-M-A0CmbiJ</recordid><startdate>202411</startdate><enddate>202411</enddate><creator>Zhao, Weihong</creator><creator>Zheng, Xirui</creator><creator>Jiang, Fengjuan</creator><creator>Liu, Jintao</creator><creator>Wang, Shuhao</creator><creator>Ou, Jiangtao</creator><general>Elsevier B.V</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>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>202411</creationdate><title>Safe concentration, unsafe effects: Impact of BPA on antioxidant function in the hepatopancreas and ovarian gene expression in oriental river prawns (Macrobrachium nipponense)</title><author>Zhao, Weihong ; Zheng, Xirui ; Jiang, Fengjuan ; Liu, Jintao ; Wang, Shuhao ; Ou, Jiangtao</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c276t-1a01c4838cca5f8c1203fe5c857725a6485206115bd0af46e1582d8c118161243</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>acute exposure</topic><topic>Acute lethal effect</topic><topic>Animals</topic><topic>antioxidant activity</topic><topic>antioxidant enzymes</topic><topic>Antioxidant reductase</topic><topic>Antioxidants - metabolism</topic><topic>Benzhydryl Compounds - toxicity</topic><topic>Bisphenol A</topic><topic>catalase</topic><topic>Catalase - genetics</topic><topic>Catalase - metabolism</topic><topic>Cathepsin B</topic><topic>Cathepsin L</topic><topic>chronic exposure</topic><topic>Endocrine Disruptors - toxicity</topic><topic>endocrine-disrupting chemicals</topic><topic>Female</topic><topic>gene expression</topic><topic>Gene Expression Regulation - drug effects</topic><topic>Heat shock protein 90</topic><topic>hepatopancreas</topic><topic>Hepatopancreas - drug effects</topic><topic>Hepatopancreas - metabolism</topic><topic>HSP90 Heat-Shock Proteins - genetics</topic><topic>HSP90 Heat-Shock Proteins - metabolism</topic><topic>Macrobrachium nipponense</topic><topic>ovarian development</topic><topic>Ovary - drug effects</topic><topic>Ovary - metabolism</topic><topic>Palaemonidae - drug effects</topic><topic>Palaemonidae - genetics</topic><topic>Phenols - toxicity</topic><topic>rivers</topic><topic>superoxide dismutase</topic><topic>Superoxide Dismutase - genetics</topic><topic>Superoxide Dismutase - metabolism</topic><topic>toxicology</topic><topic>Water Pollutants, Chemical - toxicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhao, Weihong</creatorcontrib><creatorcontrib>Zheng, Xirui</creatorcontrib><creatorcontrib>Jiang, Fengjuan</creatorcontrib><creatorcontrib>Liu, Jintao</creatorcontrib><creatorcontrib>Wang, Shuhao</creatorcontrib><creatorcontrib>Ou, Jiangtao</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Aquatic toxicology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhao, Weihong</au><au>Zheng, Xirui</au><au>Jiang, Fengjuan</au><au>Liu, Jintao</au><au>Wang, Shuhao</au><au>Ou, Jiangtao</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Safe concentration, unsafe effects: Impact of BPA on antioxidant function in the hepatopancreas and ovarian gene expression in oriental river prawns (Macrobrachium nipponense)</atitle><jtitle>Aquatic toxicology</jtitle><addtitle>Aquat Toxicol</addtitle><date>2024-11</date><risdate>2024</risdate><volume>276</volume><spage>107103</spage><pages>107103-</pages><artnum>107103</artnum><issn>0166-445X</issn><issn>1879-1514</issn><eissn>1879-1514</eissn><abstract><![CDATA[•The 24hLC50 and 48hLC50 of BPA for M. nipponense are 80.59 and 63.90 mg/L.•BPA enhances ovarian gene expression, causing precocious puberty and miniaturization.•Even safe-level BPA causes oxidative stress, affecting ovarian development.•The biological damage caused by BPA is reversible. This study investigated the effects of Bisphenol A (BPA), a common endocrine-disrupting chemical, on the antioxidant enzyme activities in the hepatopancreas and the expression of genes related to ovarian development in oriental river prawns (Macrobrachium nipponense). The 24hLC50 and 48hLC50 values for BPA were 80.59 mg/L and 63.90 mg/L, respectively, with a safe concentration of 12.06 mg/L. Prawns were exposed to low (4.85 mg/L), safe (12.06 mg/L), and high (30.00 mg/L) concentrations of BPA for 10 days to measure enzyme activities, and for 20 days followed by 7 days in BPA-free water to measure gene expression. Short-term exposure (12 h, 1d, 3d) to low concentration BPA did not significantly affect superoxide dismutase (SOD) activity in the hepatopancreas (P > 0.05), but long-term exposure (6d, 10d) significantly reduced SOD activity (P < 0.05). Catalase (CAT) activity showed no significant changes throughout the low concentration exposure period (P > 0.05). At safe and high concentrations, SOD and CAT activities significantly decreased after 12 h of exposure (P < 0.05). BPA affected heat shock protein 90 (HSP90) expression in the ovary, with low concentration BPA significantly upregulating HSP90 after 1 day (P < 0.05), but returning to normal levels after 10 and 20 days. At the safe concentration, HSP90 was significantly upregulated at all three sampling points (1d, 10d, 20d) (P < 0.05), while high concentration exposure led to significant upregulation only on day 10 (P < 0.05). Low concentration BPA had no significant effect on Cathepsin B (CB) and Cathepsin L (CL) gene expression in the ovaries (P > 0.05). However, safe concentration exposure promoted CB expression on days 1, 10, and 20 (P < 0.05), while high concentration exposure significantly increased CB expression on day 1 (P < 0.05), with levels returning to normal on days 10 and 20. CL expression significantly increased after 20 days of exposure to both safe and high concentrations (P < 0.05). Gene expression levels in the ovaries returned to normal after transfer to BPA-free water, with HSP90 and CB normalizing by day 1, and CL by day 7. These results indicate that even safe concentrations of BPA impose stress on the hepatopancreas and increase the expression of HSP90, CB, and CL genes in the ovaries, affecting ovarian development. And, these effects are reversible within a certain period after the removal of BPA.]]></abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>39305710</pmid><doi>10.1016/j.aquatox.2024.107103</doi></addata></record>
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subjects acute exposure
Acute lethal effect
Animals
antioxidant activity
antioxidant enzymes
Antioxidant reductase
Antioxidants - metabolism
Benzhydryl Compounds - toxicity
Bisphenol A
catalase
Catalase - genetics
Catalase - metabolism
Cathepsin B
Cathepsin L
chronic exposure
Endocrine Disruptors - toxicity
endocrine-disrupting chemicals
Female
gene expression
Gene Expression Regulation - drug effects
Heat shock protein 90
hepatopancreas
Hepatopancreas - drug effects
Hepatopancreas - metabolism
HSP90 Heat-Shock Proteins - genetics
HSP90 Heat-Shock Proteins - metabolism
Macrobrachium nipponense
ovarian development
Ovary - drug effects
Ovary - metabolism
Palaemonidae - drug effects
Palaemonidae - genetics
Phenols - toxicity
rivers
superoxide dismutase
Superoxide Dismutase - genetics
Superoxide Dismutase - metabolism
toxicology
Water Pollutants, Chemical - toxicity
title Safe concentration, unsafe effects: Impact of BPA on antioxidant function in the hepatopancreas and ovarian gene expression in oriental river prawns (Macrobrachium nipponense)
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