An assessment of serum‐dependent impacts on intracellular accumulation and genomic response of per‐ and polyfluoroalkyl substances in a placental trophoblast model
Per‐ and polyfluoroalkyl substances (PFAS), a class of environmental contaminants, have been detected in human placenta and cord blood. The mechanisms driving PFAS‐induced effects on the placenta and adverse pregnancy outcomes are not well understood. This study investigated the impact of perfluoroo...
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| Veröffentlicht in: | Environmental toxicology 2020-12, Vol.35 (12), p.1395-1405 |
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| creator | Bangma, Jacqueline Szilagyi, John Blake, Bevin E. Plazas, Cinthya Kepper, Stewart Fenton, Suzanne E. Fry, Rebecca |
| description | Per‐ and polyfluoroalkyl substances (PFAS), a class of environmental contaminants, have been detected in human placenta and cord blood. The mechanisms driving PFAS‐induced effects on the placenta and adverse pregnancy outcomes are not well understood. This study investigated the impact of perfluorooctanesulfonic acid (PFOS), perfluorooctanoic acid (PFOA), and a replacement PFAS known as hexafluoropropylene oxide dimer acid (HFPO‐DA, tradename GenX) on placental trophoblasts in vitro. Several key factors were addressed. First, PFAS levels in cell culture reagents at baseline were quantified. Second, the role of supplemental media serum in intracellular accumulation of PFAS in a human trophoblast (JEG3) cell line was established. Finally, the impact of PFAS on the expression of 96 genes involved in proper placental function in JEG3 cells was evaluated. The results revealed that serum‐free media (SFM) contained no detectable PFAS. In contrast, fetal bovine serum‐supplemented media (SSM) contained PFNA, PFUdA, PFTrDA, and 6:2 FTS, but these PFAS were not detected internally in cells. Intracellular accumulation following 24 hr treatments was significantly higher when cultured in SFM compared to SSM for PFOS and PFOA, but not HFPO‐DA. Treatment with PFAS was associated with gene expression changes (n = 32) in pathways vital to placental function, including viability, syncytialization, inflammation, transport, and invasion/mesenchymal transition. Among the most robust PFAS‐associated changes were those observed in the known apoptosis‐related genes, BAD and BAX. These results suggest a complex relationship between PFAS, in vitro culture conditions, and altered expression of key genes necessary for proper placentation. |
| doi_str_mv | 10.1002/tox.23004 |
| format | Article |
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The mechanisms driving PFAS‐induced effects on the placenta and adverse pregnancy outcomes are not well understood. This study investigated the impact of perfluorooctanesulfonic acid (PFOS), perfluorooctanoic acid (PFOA), and a replacement PFAS known as hexafluoropropylene oxide dimer acid (HFPO‐DA, tradename GenX) on placental trophoblasts in vitro. Several key factors were addressed. First, PFAS levels in cell culture reagents at baseline were quantified. Second, the role of supplemental media serum in intracellular accumulation of PFAS in a human trophoblast (JEG3) cell line was established. Finally, the impact of PFAS on the expression of 96 genes involved in proper placental function in JEG3 cells was evaluated. The results revealed that serum‐free media (SFM) contained no detectable PFAS. In contrast, fetal bovine serum‐supplemented media (SSM) contained PFNA, PFUdA, PFTrDA, and 6:2 FTS, but these PFAS were not detected internally in cells. Intracellular accumulation following 24 hr treatments was significantly higher when cultured in SFM compared to SSM for PFOS and PFOA, but not HFPO‐DA. Treatment with PFAS was associated with gene expression changes (n = 32) in pathways vital to placental function, including viability, syncytialization, inflammation, transport, and invasion/mesenchymal transition. Among the most robust PFAS‐associated changes were those observed in the known apoptosis‐related genes, BAD and BAX. These results suggest a complex relationship between PFAS, in vitro culture conditions, and altered expression of key genes necessary for proper placentation.</description><identifier>ISSN: 1520-4081</identifier><identifier>EISSN: 1522-7278</identifier><identifier>DOI: 10.1002/tox.23004</identifier><identifier>PMID: 32790152</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Accumulation ; Alkanesulfonic Acids - blood ; Alkanesulfonic Acids - metabolism ; Alkanesulfonic Acids - toxicity ; Apoptosis ; Apoptosis - drug effects ; Apoptosis - genetics ; Bioaccumulation - drug effects ; Bioaccumulation - genetics ; Caprylates - blood ; Caprylates - metabolism ; Caprylates - toxicity ; Cell culture ; Cell Culture Techniques ; Cell Line, Tumor ; Cell Survival - drug effects ; Cell Survival - genetics ; Cells ; Contaminants ; Cord blood ; Culture Media, Serum-Free ; Dimers ; Female ; Fluorocarbons - blood ; Fluorocarbons - metabolism ; Fluorocarbons - toxicity ; Gene expression ; Gene Expression - drug effects ; Genes ; GenX ; Humans ; in vitro ; Intracellular ; Mesenchyme ; Perfluorooctane sulfonic acid ; Perfluorooctanoic acid ; PFOA ; PFOS ; Placenta ; Placenta - drug effects ; Placenta - metabolism ; Pregnancy ; Reagents ; RNA, Messenger - genetics ; Serum ; Serum - chemistry ; Trophoblasts ; Trophoblasts - drug effects ; Trophoblasts - metabolism</subject><ispartof>Environmental toxicology, 2020-12, Vol.35 (12), p.1395-1405</ispartof><rights>2020 Wiley Periodicals LLC</rights><rights>2020 Wiley Periodicals LLC.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4254-860edc91a3dd30278693485e15d73596f945d3498f45f507feb8f1c603f6876f3</citedby><cites>FETCH-LOGICAL-c4254-860edc91a3dd30278693485e15d73596f945d3498f45f507feb8f1c603f6876f3</cites><orcidid>0000-0003-1512-173X ; 0000-0002-4876-2827 ; 0000-0003-0899-9018</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Ftox.23004$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Ftox.23004$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32790152$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bangma, Jacqueline</creatorcontrib><creatorcontrib>Szilagyi, John</creatorcontrib><creatorcontrib>Blake, Bevin E.</creatorcontrib><creatorcontrib>Plazas, Cinthya</creatorcontrib><creatorcontrib>Kepper, Stewart</creatorcontrib><creatorcontrib>Fenton, Suzanne E.</creatorcontrib><creatorcontrib>Fry, Rebecca</creatorcontrib><title>An assessment of serum‐dependent impacts on intracellular accumulation and genomic response of per‐ and polyfluoroalkyl substances in a placental trophoblast model</title><title>Environmental toxicology</title><addtitle>Environ Toxicol</addtitle><description>Per‐ and polyfluoroalkyl substances (PFAS), a class of environmental contaminants, have been detected in human placenta and cord blood. The mechanisms driving PFAS‐induced effects on the placenta and adverse pregnancy outcomes are not well understood. This study investigated the impact of perfluorooctanesulfonic acid (PFOS), perfluorooctanoic acid (PFOA), and a replacement PFAS known as hexafluoropropylene oxide dimer acid (HFPO‐DA, tradename GenX) on placental trophoblasts in vitro. Several key factors were addressed. First, PFAS levels in cell culture reagents at baseline were quantified. Second, the role of supplemental media serum in intracellular accumulation of PFAS in a human trophoblast (JEG3) cell line was established. Finally, the impact of PFAS on the expression of 96 genes involved in proper placental function in JEG3 cells was evaluated. The results revealed that serum‐free media (SFM) contained no detectable PFAS. In contrast, fetal bovine serum‐supplemented media (SSM) contained PFNA, PFUdA, PFTrDA, and 6:2 FTS, but these PFAS were not detected internally in cells. Intracellular accumulation following 24 hr treatments was significantly higher when cultured in SFM compared to SSM for PFOS and PFOA, but not HFPO‐DA. Treatment with PFAS was associated with gene expression changes (n = 32) in pathways vital to placental function, including viability, syncytialization, inflammation, transport, and invasion/mesenchymal transition. Among the most robust PFAS‐associated changes were those observed in the known apoptosis‐related genes, BAD and BAX. These results suggest a complex relationship between PFAS, in vitro culture conditions, and altered expression of key genes necessary for proper placentation.</description><subject>Accumulation</subject><subject>Alkanesulfonic Acids - blood</subject><subject>Alkanesulfonic Acids - metabolism</subject><subject>Alkanesulfonic Acids - toxicity</subject><subject>Apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>Apoptosis - genetics</subject><subject>Bioaccumulation - drug effects</subject><subject>Bioaccumulation - genetics</subject><subject>Caprylates - blood</subject><subject>Caprylates - metabolism</subject><subject>Caprylates - toxicity</subject><subject>Cell culture</subject><subject>Cell Culture Techniques</subject><subject>Cell Line, Tumor</subject><subject>Cell Survival - drug effects</subject><subject>Cell Survival - genetics</subject><subject>Cells</subject><subject>Contaminants</subject><subject>Cord blood</subject><subject>Culture Media, Serum-Free</subject><subject>Dimers</subject><subject>Female</subject><subject>Fluorocarbons - blood</subject><subject>Fluorocarbons - metabolism</subject><subject>Fluorocarbons - toxicity</subject><subject>Gene expression</subject><subject>Gene Expression - drug effects</subject><subject>Genes</subject><subject>GenX</subject><subject>Humans</subject><subject>in vitro</subject><subject>Intracellular</subject><subject>Mesenchyme</subject><subject>Perfluorooctane sulfonic acid</subject><subject>Perfluorooctanoic acid</subject><subject>PFOA</subject><subject>PFOS</subject><subject>Placenta</subject><subject>Placenta - drug effects</subject><subject>Placenta - metabolism</subject><subject>Pregnancy</subject><subject>Reagents</subject><subject>RNA, Messenger - genetics</subject><subject>Serum</subject><subject>Serum - chemistry</subject><subject>Trophoblasts</subject><subject>Trophoblasts - drug effects</subject><subject>Trophoblasts - metabolism</subject><issn>1520-4081</issn><issn>1522-7278</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUtuFDEQhi0EIiGw4ALIEisWnbjbj-5eRlF4SJGySaTsWh67DB3ctnG5BbPLEbgF9-IkeGYCO1Yu-f_0lVQ_Ia9bdtoy1p2V-OO044yJJ-S4lV3X9F0_PN3PrBFsaI_IC8R7xtiopHpOjnjXj6ymx-TXeaAaERAXCIVGRxHyuvx--GkhQbC7z3lJ2hSkMdA5lKwNeL96nak2Zl3qVOYa6WDpZwhxmQ3NgCkGhJ0vQa62fZyi3zq_xhy1_7r1FNcNFh0MYBVTTZOv7lC0pyXH9CVuvMZCl2jBvyTPnPYIrx7fE3L7_vLm4mNzdf3h08X5VWNEJ0UzKAbWjK3m1nJWr6BGLgYJrbQ9l6Nyo5CWi3FwQjrJegebwbVGMe7U0CvHT8jbgzfl-G0FLNN9XHOoK6dOyH4QivW8Uu8OlMkRMYObUp4XnbdTy6ZdJVOtZNpXUtk3j8Z1s4D9R_7toAJnB-D77GH7f9N0c313UP4BT6ebOw</recordid><startdate>202012</startdate><enddate>202012</enddate><creator>Bangma, Jacqueline</creator><creator>Szilagyi, John</creator><creator>Blake, Bevin E.</creator><creator>Plazas, Cinthya</creator><creator>Kepper, Stewart</creator><creator>Fenton, Suzanne E.</creator><creator>Fry, Rebecca</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</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>7QH</scope><scope>7ST</scope><scope>7TN</scope><scope>7U7</scope><scope>7UA</scope><scope>C1K</scope><scope>F1W</scope><scope>H97</scope><scope>K9.</scope><scope>L.G</scope><scope>M7N</scope><scope>SOI</scope><orcidid>https://orcid.org/0000-0003-1512-173X</orcidid><orcidid>https://orcid.org/0000-0002-4876-2827</orcidid><orcidid>https://orcid.org/0000-0003-0899-9018</orcidid></search><sort><creationdate>202012</creationdate><title>An assessment of serum‐dependent impacts on intracellular accumulation and genomic response of per‐ and polyfluoroalkyl substances in a placental trophoblast model</title><author>Bangma, Jacqueline ; 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The mechanisms driving PFAS‐induced effects on the placenta and adverse pregnancy outcomes are not well understood. This study investigated the impact of perfluorooctanesulfonic acid (PFOS), perfluorooctanoic acid (PFOA), and a replacement PFAS known as hexafluoropropylene oxide dimer acid (HFPO‐DA, tradename GenX) on placental trophoblasts in vitro. Several key factors were addressed. First, PFAS levels in cell culture reagents at baseline were quantified. Second, the role of supplemental media serum in intracellular accumulation of PFAS in a human trophoblast (JEG3) cell line was established. Finally, the impact of PFAS on the expression of 96 genes involved in proper placental function in JEG3 cells was evaluated. The results revealed that serum‐free media (SFM) contained no detectable PFAS. In contrast, fetal bovine serum‐supplemented media (SSM) contained PFNA, PFUdA, PFTrDA, and 6:2 FTS, but these PFAS were not detected internally in cells. Intracellular accumulation following 24 hr treatments was significantly higher when cultured in SFM compared to SSM for PFOS and PFOA, but not HFPO‐DA. Treatment with PFAS was associated with gene expression changes (n = 32) in pathways vital to placental function, including viability, syncytialization, inflammation, transport, and invasion/mesenchymal transition. Among the most robust PFAS‐associated changes were those observed in the known apoptosis‐related genes, BAD and BAX. These results suggest a complex relationship between PFAS, in vitro culture conditions, and altered expression of key genes necessary for proper placentation.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>32790152</pmid><doi>10.1002/tox.23004</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-1512-173X</orcidid><orcidid>https://orcid.org/0000-0002-4876-2827</orcidid><orcidid>https://orcid.org/0000-0003-0899-9018</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Accumulation Alkanesulfonic Acids - blood Alkanesulfonic Acids - metabolism Alkanesulfonic Acids - toxicity Apoptosis Apoptosis - drug effects Apoptosis - genetics Bioaccumulation - drug effects Bioaccumulation - genetics Caprylates - blood Caprylates - metabolism Caprylates - toxicity Cell culture Cell Culture Techniques Cell Line, Tumor Cell Survival - drug effects Cell Survival - genetics Cells Contaminants Cord blood Culture Media, Serum-Free Dimers Female Fluorocarbons - blood Fluorocarbons - metabolism Fluorocarbons - toxicity Gene expression Gene Expression - drug effects Genes GenX Humans in vitro Intracellular Mesenchyme Perfluorooctane sulfonic acid Perfluorooctanoic acid PFOA PFOS Placenta Placenta - drug effects Placenta - metabolism Pregnancy Reagents RNA, Messenger - genetics Serum Serum - chemistry Trophoblasts Trophoblasts - drug effects Trophoblasts - metabolism |
| title | An assessment of serum‐dependent impacts on intracellular accumulation and genomic response of per‐ and polyfluoroalkyl substances in a placental trophoblast model |
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