Functional characterization of common carp (Cyprinus carpio) AHRs: Subform-specific sensitivity to dioxin and interspecies differences
Dioxins are widely known to bioaccumulate in the body and produce a wide spectrum of toxic effects on both humans and wildlife. In addition, some novel sorts of compounds that were similar in structure and effect were gradually identified and termed dioxin-like compounds (DLCs). The toxicity of diox...
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creator | Zhang, Wanglong Zhang, Chen Sha, Weilai Xue, Zhenhong Zhou, Zhiguang Ma, Yongchao Ding, Ning Gao, Peike Tian, Wenjing Zhang, Liwen Wu, Jiarun Zhao, Bin Wang, Renjun |
description | Dioxins are widely known to bioaccumulate in the body and produce a wide spectrum of toxic effects on both humans and wildlife. In addition, some novel sorts of compounds that were similar in structure and effect were gradually identified and termed dioxin-like compounds (DLCs). The toxicity of dioxins as well as DLCs is predominantly mediated by the dioxin receptor (aryl hydrocarbon receptor, AHR) in animals, which is usually differentially expressed and functionally distinct (especially the sensitivity to dioxins) among species, possibly resulting in species-specific variations in the toxicity of dioxins. Therefore, detailed functional exploration of the AHRs of a given species, such as the common carp (which is a vital wild and commercial species with a broad geological distribution) in the current study, will enable a comprehensive ecotoxicity evaluation. Through genome survey and phylogenetic analysis, we identified three AHRs (AHR1a, AHR1b, and AHR2) and two ARNTs (ARNT1 and ARNT2). AHR2 was observed to have greater expression abundance in the gill and brain, and may serve as the predominant subform. Those AHRs and ARNTs are functional, and the AHRs can be efficiently transactivated by the classical dioxin congener 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). We individually determined the EC50 values of AHR1a (0.41 ± 0.24 nM), AHR1b (12.80 ± 3.28 nM), and AHR2 (0.64 ± 0.49 nM), and found that: 1) The AHR sensitivities of common carp and zebrafish (phylogenetically close species) are relatively similar. AHR1a and the predominant form AHR2 have greater sensitivity to TCDD. 2) ARNT1 and ARNT2 do not produce different sensitivities, but with distinct induction fold, of a given AHR transactivation when cooperating as the partner; 3) Distinct AHR subforms of the same or distinct species can have even one or two orders of magnitude differences in sensitivity. In summary, the current study will add to the knowledge of AHR biology and help improve ecotoxicology research on dioxins and DLCs.
[Display omitted]
•The constitution of three common carp AHRs in this study is similar to zebrafish.•The sensitivity of AHR1b and AHR2 of common carp and zebrafish to dioxin is similar.•Common carp ARNT1 and ARNT2 may not necessarily produce different sensitivity of AHR when cooperating as the partner.•One or two orders of difference in sensitivity to dioxin can happen among distinct subforms or species. |
doi_str_mv | 10.1016/j.scitotenv.2023.163809 |
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[Display omitted]
•The constitution of three common carp AHRs in this study is similar to zebrafish.•The sensitivity of AHR1b and AHR2 of common carp and zebrafish to dioxin is similar.•Common carp ARNT1 and ARNT2 may not necessarily produce different sensitivity of AHR when cooperating as the partner.•One or two orders of difference in sensitivity to dioxin can happen among distinct subforms or species.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2023.163809</identifier><identifier>PMID: 37127157</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Aryl hydrocarbon receptor ; Cyprinus carpio ; Dioxin ; Dioxin-like compounds ; Toxic potential</subject><ispartof>The Science of the total environment, 2023-08, Vol.884, p.163809-163809, Article 163809</ispartof><rights>2023 Elsevier B.V.</rights><rights>Copyright © 2023 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c371t-e52708db1e3967f2ba5c1a81c35c4d7c85ca60590433d476026d5520d6930a583</citedby><cites>FETCH-LOGICAL-c371t-e52708db1e3967f2ba5c1a81c35c4d7c85ca60590433d476026d5520d6930a583</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.scitotenv.2023.163809$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37127157$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Wanglong</creatorcontrib><creatorcontrib>Zhang, Chen</creatorcontrib><creatorcontrib>Sha, Weilai</creatorcontrib><creatorcontrib>Xue, Zhenhong</creatorcontrib><creatorcontrib>Zhou, Zhiguang</creatorcontrib><creatorcontrib>Ma, Yongchao</creatorcontrib><creatorcontrib>Ding, Ning</creatorcontrib><creatorcontrib>Gao, Peike</creatorcontrib><creatorcontrib>Tian, Wenjing</creatorcontrib><creatorcontrib>Zhang, Liwen</creatorcontrib><creatorcontrib>Wu, Jiarun</creatorcontrib><creatorcontrib>Zhao, Bin</creatorcontrib><creatorcontrib>Wang, Renjun</creatorcontrib><title>Functional characterization of common carp (Cyprinus carpio) AHRs: Subform-specific sensitivity to dioxin and interspecies differences</title><title>The Science of the total environment</title><addtitle>Sci Total Environ</addtitle><description>Dioxins are widely known to bioaccumulate in the body and produce a wide spectrum of toxic effects on both humans and wildlife. In addition, some novel sorts of compounds that were similar in structure and effect were gradually identified and termed dioxin-like compounds (DLCs). The toxicity of dioxins as well as DLCs is predominantly mediated by the dioxin receptor (aryl hydrocarbon receptor, AHR) in animals, which is usually differentially expressed and functionally distinct (especially the sensitivity to dioxins) among species, possibly resulting in species-specific variations in the toxicity of dioxins. Therefore, detailed functional exploration of the AHRs of a given species, such as the common carp (which is a vital wild and commercial species with a broad geological distribution) in the current study, will enable a comprehensive ecotoxicity evaluation. Through genome survey and phylogenetic analysis, we identified three AHRs (AHR1a, AHR1b, and AHR2) and two ARNTs (ARNT1 and ARNT2). AHR2 was observed to have greater expression abundance in the gill and brain, and may serve as the predominant subform. Those AHRs and ARNTs are functional, and the AHRs can be efficiently transactivated by the classical dioxin congener 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). We individually determined the EC50 values of AHR1a (0.41 ± 0.24 nM), AHR1b (12.80 ± 3.28 nM), and AHR2 (0.64 ± 0.49 nM), and found that: 1) The AHR sensitivities of common carp and zebrafish (phylogenetically close species) are relatively similar. AHR1a and the predominant form AHR2 have greater sensitivity to TCDD. 2) ARNT1 and ARNT2 do not produce different sensitivities, but with distinct induction fold, of a given AHR transactivation when cooperating as the partner; 3) Distinct AHR subforms of the same or distinct species can have even one or two orders of magnitude differences in sensitivity. In summary, the current study will add to the knowledge of AHR biology and help improve ecotoxicology research on dioxins and DLCs.
[Display omitted]
•The constitution of three common carp AHRs in this study is similar to zebrafish.•The sensitivity of AHR1b and AHR2 of common carp and zebrafish to dioxin is similar.•Common carp ARNT1 and ARNT2 may not necessarily produce different sensitivity of AHR when cooperating as the partner.•One or two orders of difference in sensitivity to dioxin can happen among distinct subforms or species.</description><subject>Aryl hydrocarbon receptor</subject><subject>Cyprinus carpio</subject><subject>Dioxin</subject><subject>Dioxin-like compounds</subject><subject>Toxic potential</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqFUctuUzEQtRCIpoVfAC_L4gY_4sdlF0WUIlVC4rG2HHuucJRrB9s3Iv0AvhvfpnSLN-MZnTkzcw5CbylZUkLl-92yuFBThXhcMsL4kkquSf8MLahWfUcJk8_RgpCV7nrZqwt0WcqOtKc0fYkuuKJMUaEW6M_NFF0NKdo9dj9ttq5CDvd2LuE0YJfGsf2czQd8vTkdcohTeUhDeofXt1_LB_xt2g4pj105gAtDcLhALKGGY6gnXBP2If0OEdvocYiN_gEHpdWHATJEB-UVejHYfYHXj_EK_bj5-H1z2919-fR5s77rXFu5diCYItpvKfBeqoFtrXDUauq4cCuvnBbOSiJ6suLcr5RsMnghGPGy58QKza_Q9Zn3kNOvCUo1YygO9nsbIU3FME200JKxGarOUJdTKRkG044fbT4ZSsxsgtmZJxPMbII5m9A63zwOmbYj-Ke-f6o3wPoMgHbqMUCeiWYdfMjgqvEp_HfIX375nv4</recordid><startdate>20230801</startdate><enddate>20230801</enddate><creator>Zhang, Wanglong</creator><creator>Zhang, Chen</creator><creator>Sha, Weilai</creator><creator>Xue, Zhenhong</creator><creator>Zhou, Zhiguang</creator><creator>Ma, Yongchao</creator><creator>Ding, Ning</creator><creator>Gao, Peike</creator><creator>Tian, Wenjing</creator><creator>Zhang, Liwen</creator><creator>Wu, Jiarun</creator><creator>Zhao, Bin</creator><creator>Wang, Renjun</creator><general>Elsevier B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20230801</creationdate><title>Functional characterization of common carp (Cyprinus carpio) AHRs: Subform-specific sensitivity to dioxin and interspecies differences</title><author>Zhang, Wanglong ; Zhang, Chen ; Sha, Weilai ; Xue, Zhenhong ; Zhou, Zhiguang ; Ma, Yongchao ; Ding, Ning ; Gao, Peike ; Tian, Wenjing ; Zhang, Liwen ; Wu, Jiarun ; Zhao, Bin ; Wang, Renjun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c371t-e52708db1e3967f2ba5c1a81c35c4d7c85ca60590433d476026d5520d6930a583</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Aryl hydrocarbon receptor</topic><topic>Cyprinus carpio</topic><topic>Dioxin</topic><topic>Dioxin-like compounds</topic><topic>Toxic potential</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Wanglong</creatorcontrib><creatorcontrib>Zhang, Chen</creatorcontrib><creatorcontrib>Sha, Weilai</creatorcontrib><creatorcontrib>Xue, Zhenhong</creatorcontrib><creatorcontrib>Zhou, Zhiguang</creatorcontrib><creatorcontrib>Ma, Yongchao</creatorcontrib><creatorcontrib>Ding, Ning</creatorcontrib><creatorcontrib>Gao, Peike</creatorcontrib><creatorcontrib>Tian, Wenjing</creatorcontrib><creatorcontrib>Zhang, Liwen</creatorcontrib><creatorcontrib>Wu, Jiarun</creatorcontrib><creatorcontrib>Zhao, Bin</creatorcontrib><creatorcontrib>Wang, Renjun</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Wanglong</au><au>Zhang, Chen</au><au>Sha, Weilai</au><au>Xue, Zhenhong</au><au>Zhou, Zhiguang</au><au>Ma, Yongchao</au><au>Ding, Ning</au><au>Gao, Peike</au><au>Tian, Wenjing</au><au>Zhang, Liwen</au><au>Wu, Jiarun</au><au>Zhao, Bin</au><au>Wang, Renjun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional characterization of common carp (Cyprinus carpio) AHRs: Subform-specific sensitivity to dioxin and interspecies differences</atitle><jtitle>The Science of the total environment</jtitle><addtitle>Sci Total Environ</addtitle><date>2023-08-01</date><risdate>2023</risdate><volume>884</volume><spage>163809</spage><epage>163809</epage><pages>163809-163809</pages><artnum>163809</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Dioxins are widely known to bioaccumulate in the body and produce a wide spectrum of toxic effects on both humans and wildlife. In addition, some novel sorts of compounds that were similar in structure and effect were gradually identified and termed dioxin-like compounds (DLCs). The toxicity of dioxins as well as DLCs is predominantly mediated by the dioxin receptor (aryl hydrocarbon receptor, AHR) in animals, which is usually differentially expressed and functionally distinct (especially the sensitivity to dioxins) among species, possibly resulting in species-specific variations in the toxicity of dioxins. Therefore, detailed functional exploration of the AHRs of a given species, such as the common carp (which is a vital wild and commercial species with a broad geological distribution) in the current study, will enable a comprehensive ecotoxicity evaluation. Through genome survey and phylogenetic analysis, we identified three AHRs (AHR1a, AHR1b, and AHR2) and two ARNTs (ARNT1 and ARNT2). AHR2 was observed to have greater expression abundance in the gill and brain, and may serve as the predominant subform. Those AHRs and ARNTs are functional, and the AHRs can be efficiently transactivated by the classical dioxin congener 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). We individually determined the EC50 values of AHR1a (0.41 ± 0.24 nM), AHR1b (12.80 ± 3.28 nM), and AHR2 (0.64 ± 0.49 nM), and found that: 1) The AHR sensitivities of common carp and zebrafish (phylogenetically close species) are relatively similar. AHR1a and the predominant form AHR2 have greater sensitivity to TCDD. 2) ARNT1 and ARNT2 do not produce different sensitivities, but with distinct induction fold, of a given AHR transactivation when cooperating as the partner; 3) Distinct AHR subforms of the same or distinct species can have even one or two orders of magnitude differences in sensitivity. In summary, the current study will add to the knowledge of AHR biology and help improve ecotoxicology research on dioxins and DLCs.
[Display omitted]
•The constitution of three common carp AHRs in this study is similar to zebrafish.•The sensitivity of AHR1b and AHR2 of common carp and zebrafish to dioxin is similar.•Common carp ARNT1 and ARNT2 may not necessarily produce different sensitivity of AHR when cooperating as the partner.•One or two orders of difference in sensitivity to dioxin can happen among distinct subforms or species.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>37127157</pmid><doi>10.1016/j.scitotenv.2023.163809</doi><tpages>1</tpages></addata></record> |
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subjects | Aryl hydrocarbon receptor Cyprinus carpio Dioxin Dioxin-like compounds Toxic potential |
title | Functional characterization of common carp (Cyprinus carpio) AHRs: Subform-specific sensitivity to dioxin and interspecies differences |
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