Transcriptomic and metabolomic analyses revealed epiboly delayed mechanisms of 2,5-dichloro-1, 4-benuinone on zebrafish embryos
2,5-Dichloro-1,4-benzenediol (2,5-DCBQ) is a putative disinfection by-product that belongs to the halogenated benzoquinone class. However, its developmental toxicity and related mechanism remained unclarified. In our study, we used zebrafish embryos as the model and exposed them to graded concentrat...
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description | 2,5-Dichloro-1,4-benzenediol (2,5-DCBQ) is a putative disinfection by-product that belongs to the halogenated benzoquinone class. However, its developmental toxicity and related mechanism remained unclarified. In our study, we used zebrafish embryos as the model and exposed them to graded concentrations of 2,5-DCBQ (100, 200, 300, 400 μg/L). We found that the rate of epiboly abnormalities increased significantly in a concentration-dependent manner. The results of whole-mount in situ hybridization (WISH) indicated that the expression patterns and levels of
chordin
(dorsoventral marker),
foxa2
(endodermal marker),
eve1
(ventral mesodermal marker), and
foxb1a
(ectodermal marker) were altered, suggesting that 2,5-DCBQ might affect the germ layer development of zebrafish embryos. Integrated transcriptomic and metabolomic analyses were adopted to explore the molecular mechanisms of embryonic developmental delays. The results showed that 2,5-DCBQ exposure induced 1163 differentially expressed genes (DEGs) and 37 differential metabolites (DEMs). Bioinformatic analysis enriched the most affected molecular pathways (Wnt signaling pathway, cell adhesion molecules, actin cytoskeleton regulation) and metabolic pathways (purine metabolism, aminoacyl-tRNA biosynthesis, arginine and proline metabolism) in zebrafish embryos. To summarize, our findings broadened the molecular mechanisms of 2,5-DCBQ embryotoxicity through multi-omics and bioinformatic analyses.
Graphical Abstract |
doi_str_mv | 10.1007/s11356-023-27145-4 |
format | Article |
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chordin
(dorsoventral marker),
foxa2
(endodermal marker),
eve1
(ventral mesodermal marker), and
foxb1a
(ectodermal marker) were altered, suggesting that 2,5-DCBQ might affect the germ layer development of zebrafish embryos. Integrated transcriptomic and metabolomic analyses were adopted to explore the molecular mechanisms of embryonic developmental delays. The results showed that 2,5-DCBQ exposure induced 1163 differentially expressed genes (DEGs) and 37 differential metabolites (DEMs). Bioinformatic analysis enriched the most affected molecular pathways (Wnt signaling pathway, cell adhesion molecules, actin cytoskeleton regulation) and metabolic pathways (purine metabolism, aminoacyl-tRNA biosynthesis, arginine and proline metabolism) in zebrafish embryos. To summarize, our findings broadened the molecular mechanisms of 2,5-DCBQ embryotoxicity through multi-omics and bioinformatic analyses.
Graphical Abstract</description><identifier>ISSN: 1614-7499</identifier><identifier>ISSN: 0944-1344</identifier><identifier>EISSN: 1614-7499</identifier><identifier>DOI: 10.1007/s11356-023-27145-4</identifier><identifier>PMID: 37165267</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Abnormalities ; Actin ; Animals ; Aquatic Pollution ; arginine ; Atmospheric Protection/Air Quality Control/Air Pollution ; Benzoquinone ; Benzoquinones ; Biomarkers ; Biosynthesis ; byproducts ; Cell adhesion ; Cell adhesion molecules ; Chordin ; class ; Cytoskeleton ; Danio rerio ; Disinfection ; Earth and Environmental Science ; Ecotoxicology ; ectoderm ; Embryo, Nonmammalian - metabolism ; Embryos ; embryotoxicity ; Environment ; Environmental Chemistry ; Environmental Health ; Environmental science ; gene expression regulation ; Hybridization ; Metabolic pathways ; Metabolism ; Metabolites ; Metabolomics ; microfilaments ; Molecular modelling ; multiomics ; proline ; Report writing ; Research Article ; Signal transduction ; Toxicity ; Transcriptome ; Transcriptomics ; tRNA Arg ; tRNA Pro ; Waste Water Technology ; Water Management ; Water Pollutants, Chemical - toxicity ; Water Pollution Control ; Wnt protein ; Zebrafish</subject><ispartof>Environmental science and pollution research international, 2023-06, Vol.30 (27), p.71360-71370</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c359t-75734d81fc0dd9deec6c0bba513e963c2ae4743635a0add0772019119b684ae63</cites><orcidid>0000-0001-8274-0747</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s11356-023-27145-4$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s11356-023-27145-4$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37165267$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Yuanyao</creatorcontrib><creatorcontrib>Wang, Jingming</creatorcontrib><creatorcontrib>Yu, Zhiquan</creatorcontrib><creatorcontrib>Xiao, Lin</creatorcontrib><creatorcontrib>Xu, Jia</creatorcontrib><creatorcontrib>Zhao, Kai</creatorcontrib><creatorcontrib>Zhang, Huiping</creatorcontrib><creatorcontrib>Shang, Xuejun</creatorcontrib><creatorcontrib>Liu, Chunyan</creatorcontrib><title>Transcriptomic and metabolomic analyses revealed epiboly delayed mechanisms of 2,5-dichloro-1, 4-benuinone on zebrafish embryos</title><title>Environmental science and pollution research international</title><addtitle>Environ Sci Pollut Res</addtitle><addtitle>Environ Sci Pollut Res Int</addtitle><description>2,5-Dichloro-1,4-benzenediol (2,5-DCBQ) is a putative disinfection by-product that belongs to the halogenated benzoquinone class. However, its developmental toxicity and related mechanism remained unclarified. In our study, we used zebrafish embryos as the model and exposed them to graded concentrations of 2,5-DCBQ (100, 200, 300, 400 μg/L). We found that the rate of epiboly abnormalities increased significantly in a concentration-dependent manner. The results of whole-mount in situ hybridization (WISH) indicated that the expression patterns and levels of
chordin
(dorsoventral marker),
foxa2
(endodermal marker),
eve1
(ventral mesodermal marker), and
foxb1a
(ectodermal marker) were altered, suggesting that 2,5-DCBQ might affect the germ layer development of zebrafish embryos. Integrated transcriptomic and metabolomic analyses were adopted to explore the molecular mechanisms of embryonic developmental delays. The results showed that 2,5-DCBQ exposure induced 1163 differentially expressed genes (DEGs) and 37 differential metabolites (DEMs). Bioinformatic analysis enriched the most affected molecular pathways (Wnt signaling pathway, cell adhesion molecules, actin cytoskeleton regulation) and metabolic pathways (purine metabolism, aminoacyl-tRNA biosynthesis, arginine and proline metabolism) in zebrafish embryos. To summarize, our findings broadened the molecular mechanisms of 2,5-DCBQ embryotoxicity through multi-omics and bioinformatic analyses.
Graphical Abstract</description><subject>Abnormalities</subject><subject>Actin</subject><subject>Animals</subject><subject>Aquatic Pollution</subject><subject>arginine</subject><subject>Atmospheric Protection/Air Quality Control/Air Pollution</subject><subject>Benzoquinone</subject><subject>Benzoquinones</subject><subject>Biomarkers</subject><subject>Biosynthesis</subject><subject>byproducts</subject><subject>Cell adhesion</subject><subject>Cell adhesion molecules</subject><subject>Chordin</subject><subject>class</subject><subject>Cytoskeleton</subject><subject>Danio rerio</subject><subject>Disinfection</subject><subject>Earth and Environmental Science</subject><subject>Ecotoxicology</subject><subject>ectoderm</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>Embryos</subject><subject>embryotoxicity</subject><subject>Environment</subject><subject>Environmental Chemistry</subject><subject>Environmental Health</subject><subject>Environmental science</subject><subject>gene expression regulation</subject><subject>Hybridization</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metabolomics</subject><subject>microfilaments</subject><subject>Molecular modelling</subject><subject>multiomics</subject><subject>proline</subject><subject>Report writing</subject><subject>Research Article</subject><subject>Signal transduction</subject><subject>Toxicity</subject><subject>Transcriptome</subject><subject>Transcriptomics</subject><subject>tRNA Arg</subject><subject>tRNA Pro</subject><subject>Waste Water Technology</subject><subject>Water Management</subject><subject>Water Pollutants, Chemical - toxicity</subject><subject>Water Pollution Control</subject><subject>Wnt protein</subject><subject>Zebrafish</subject><issn>1614-7499</issn><issn>0944-1344</issn><issn>1614-7499</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFkU1v1DAQhiNERUvhD3BAlrhwqIvHn_ERVUCRKnEpZ8uxJ2yqxF7sDVJ66V8nyy4f4gCn8WieeUfy0zQvgF0CY-ZNBRBKU8YF5QakovJRcwYaJDXS2sd_vE-bp7XeMcaZ5eZJcyoMaMW1OWsebotPNZRhu8vTEIhPkUy4810ej70fl4qVFPyGfsRIcDusw4VEHP2CezpsfBrqVEnuCb9QNA5hM-aSKVwQSTtM85ByQpITuceu-H6oG4JTV5ZcnzUnvR8rPj_W8-bz-3e3V9f05tOHj1dvb2gQyu6oUUbI2EIfWIw2IgYdWNd5BQKtFoF7lEYKLZRnPkZmDGdgAWynW-lRi_Pm9SF3W_LXGevOTUMNOI4-YZ6rE6AEWAUM_ovyFrhiyrR8RV_9hd7luaxftqc4WNsy2N_mByqUXGvB3m3LMPmyOGBub9IdTLrVpPth0sl16eUxeu4mjL9WfqpbAXEA6jpKX7D8vv2P2O_XFakg</recordid><startdate>20230601</startdate><enddate>20230601</enddate><creator>Chen, Yuanyao</creator><creator>Wang, Jingming</creator><creator>Yu, Zhiquan</creator><creator>Xiao, Lin</creator><creator>Xu, Jia</creator><creator>Zhao, Kai</creator><creator>Zhang, Huiping</creator><creator>Shang, Xuejun</creator><creator>Liu, Chunyan</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature 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>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7T7</scope><scope>7TV</scope><scope>7U7</scope><scope>7WY</scope><scope>7WZ</scope><scope>7X7</scope><scope>7XB</scope><scope>87Z</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8FL</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>BEZIV</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FRNLG</scope><scope>FYUFA</scope><scope>F~G</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K60</scope><scope>K6~</scope><scope>K9.</scope><scope>L.-</scope><scope>M0C</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7N</scope><scope>P64</scope><scope>PATMY</scope><scope>PQBIZ</scope><scope>PQBZA</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>Q9U</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0001-8274-0747</orcidid></search><sort><creationdate>20230601</creationdate><title>Transcriptomic and metabolomic analyses revealed epiboly delayed mechanisms of 2,5-dichloro-1, 4-benuinone on zebrafish embryos</title><author>Chen, Yuanyao ; Wang, Jingming ; Yu, Zhiquan ; Xiao, Lin ; Xu, Jia ; Zhao, Kai ; Zhang, Huiping ; Shang, Xuejun ; Liu, Chunyan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c359t-75734d81fc0dd9deec6c0bba513e963c2ae4743635a0add0772019119b684ae63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Abnormalities</topic><topic>Actin</topic><topic>Animals</topic><topic>Aquatic Pollution</topic><topic>arginine</topic><topic>Atmospheric Protection/Air Quality Control/Air Pollution</topic><topic>Benzoquinone</topic><topic>Benzoquinones</topic><topic>Biomarkers</topic><topic>Biosynthesis</topic><topic>byproducts</topic><topic>Cell adhesion</topic><topic>Cell adhesion molecules</topic><topic>Chordin</topic><topic>class</topic><topic>Cytoskeleton</topic><topic>Danio rerio</topic><topic>Disinfection</topic><topic>Earth and Environmental Science</topic><topic>Ecotoxicology</topic><topic>ectoderm</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>Embryos</topic><topic>embryotoxicity</topic><topic>Environment</topic><topic>Environmental Chemistry</topic><topic>Environmental Health</topic><topic>Environmental science</topic><topic>gene expression regulation</topic><topic>Hybridization</topic><topic>Metabolic pathways</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Metabolomics</topic><topic>microfilaments</topic><topic>Molecular modelling</topic><topic>multiomics</topic><topic>proline</topic><topic>Report writing</topic><topic>Research Article</topic><topic>Signal transduction</topic><topic>Toxicity</topic><topic>Transcriptome</topic><topic>Transcriptomics</topic><topic>tRNA Arg</topic><topic>tRNA Pro</topic><topic>Waste Water Technology</topic><topic>Water Management</topic><topic>Water Pollutants, Chemical - toxicity</topic><topic>Water Pollution Control</topic><topic>Wnt protein</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Yuanyao</creatorcontrib><creatorcontrib>Wang, Jingming</creatorcontrib><creatorcontrib>Yu, Zhiquan</creatorcontrib><creatorcontrib>Xiao, Lin</creatorcontrib><creatorcontrib>Xu, Jia</creatorcontrib><creatorcontrib>Zhao, Kai</creatorcontrib><creatorcontrib>Zhang, Huiping</creatorcontrib><creatorcontrib>Shang, Xuejun</creatorcontrib><creatorcontrib>Liu, Chunyan</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>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Pollution Abstracts</collection><collection>Toxicology Abstracts</collection><collection>ABI/INFORM Collection</collection><collection>ABI/INFORM Global (PDF only)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>ABI/INFORM Global (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ABI/INFORM Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>Business Premium Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Business Premium Collection (Alumni)</collection><collection>Health Research Premium Collection</collection><collection>ABI/INFORM Global (Corporate)</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Business Collection (Alumni Edition)</collection><collection>ProQuest Business Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ABI/INFORM Professional Advanced</collection><collection>ABI/INFORM Global</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Business</collection><collection>ProQuest One Business (Alumni)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Environmental science and pollution research international</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Yuanyao</au><au>Wang, Jingming</au><au>Yu, Zhiquan</au><au>Xiao, Lin</au><au>Xu, Jia</au><au>Zhao, Kai</au><au>Zhang, Huiping</au><au>Shang, Xuejun</au><au>Liu, Chunyan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptomic and metabolomic analyses revealed epiboly delayed mechanisms of 2,5-dichloro-1, 4-benuinone on zebrafish embryos</atitle><jtitle>Environmental science and pollution research international</jtitle><stitle>Environ Sci Pollut Res</stitle><addtitle>Environ Sci Pollut Res Int</addtitle><date>2023-06-01</date><risdate>2023</risdate><volume>30</volume><issue>27</issue><spage>71360</spage><epage>71370</epage><pages>71360-71370</pages><issn>1614-7499</issn><issn>0944-1344</issn><eissn>1614-7499</eissn><abstract>2,5-Dichloro-1,4-benzenediol (2,5-DCBQ) is a putative disinfection by-product that belongs to the halogenated benzoquinone class. However, its developmental toxicity and related mechanism remained unclarified. In our study, we used zebrafish embryos as the model and exposed them to graded concentrations of 2,5-DCBQ (100, 200, 300, 400 μg/L). We found that the rate of epiboly abnormalities increased significantly in a concentration-dependent manner. The results of whole-mount in situ hybridization (WISH) indicated that the expression patterns and levels of
chordin
(dorsoventral marker),
foxa2
(endodermal marker),
eve1
(ventral mesodermal marker), and
foxb1a
(ectodermal marker) were altered, suggesting that 2,5-DCBQ might affect the germ layer development of zebrafish embryos. Integrated transcriptomic and metabolomic analyses were adopted to explore the molecular mechanisms of embryonic developmental delays. The results showed that 2,5-DCBQ exposure induced 1163 differentially expressed genes (DEGs) and 37 differential metabolites (DEMs). Bioinformatic analysis enriched the most affected molecular pathways (Wnt signaling pathway, cell adhesion molecules, actin cytoskeleton regulation) and metabolic pathways (purine metabolism, aminoacyl-tRNA biosynthesis, arginine and proline metabolism) in zebrafish embryos. To summarize, our findings broadened the molecular mechanisms of 2,5-DCBQ embryotoxicity through multi-omics and bioinformatic analyses.
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subjects | Abnormalities Actin Animals Aquatic Pollution arginine Atmospheric Protection/Air Quality Control/Air Pollution Benzoquinone Benzoquinones Biomarkers Biosynthesis byproducts Cell adhesion Cell adhesion molecules Chordin class Cytoskeleton Danio rerio Disinfection Earth and Environmental Science Ecotoxicology ectoderm Embryo, Nonmammalian - metabolism Embryos embryotoxicity Environment Environmental Chemistry Environmental Health Environmental science gene expression regulation Hybridization Metabolic pathways Metabolism Metabolites Metabolomics microfilaments Molecular modelling multiomics proline Report writing Research Article Signal transduction Toxicity Transcriptome Transcriptomics tRNA Arg tRNA Pro Waste Water Technology Water Management Water Pollutants, Chemical - toxicity Water Pollution Control Wnt protein Zebrafish |
title | Transcriptomic and metabolomic analyses revealed epiboly delayed mechanisms of 2,5-dichloro-1, 4-benuinone on zebrafish embryos |
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