Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation
Benzo(a)pyrene (BP) is an environmental contaminant known to favor airway inflammation likely through up-regulation of pro-inflammatory cytokines. The present study was designed to characterize its effects toward interleukin-8 (IL-8), a well-established pulmonary inflammatory cytokine. In primary hu...
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| Veröffentlicht in: | Toxicology letters 2008-03, Vol.177 (2), p.130-137 |
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| creator | Podechard, Normand Lecureur, Valérie Le Ferrec, Eric Guenon, Isabelle Sparfel, Lydie Gilot, David Gordon, John R. Lagente, Vincent Fardel, Olivier |
| description | Benzo(a)pyrene (BP) is an environmental contaminant known to favor airway inflammation likely through up-regulation of pro-inflammatory cytokines. The present study was designed to characterize its effects toward interleukin-8 (IL-8), a well-established pulmonary inflammatory cytokine. In primary human macrophages, BP was shown to induce IL-8 expression at both mRNA and secretion levels in a dose-dependent manner. Such an up-regulation was likely linked to aryl hydrocarbon receptor (AhR)-activation since BP-mediated IL-8 induction was reduced after AhR expression knock-down through RNA interference. Moreover, electrophoretic mobility shift assays (EMSAs) and chromatin immunoprecipitation experiments showed BP-triggered binding of AhR to a consensus xenobiotic responsive element (XRE) found in the human IL-8 promoter. Finally, BP administration to mice led to over-expression of keratinocyte chemoattractant (KC), the murine functional homologue of IL-8, in lung. It also triggered the recruitment of neutrophils in bronchoalveolar lavage (BAL) fluids, which was however fully abolished in the presence of a chemical antagonist of the KC/IL-8 receptors CXCR1/CXCR2, thus supporting the functional and crucial involvement of KC in BP-induced lung inflammation. Overall, these data highlight an AhR-dependent regulation of IL-8 in response to BP that likely contributes to the airway inflammatory effects of this environmental chemical. |
| doi_str_mv | 10.1016/j.toxlet.2008.01.006 |
| format | Article |
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The present study was designed to characterize its effects toward interleukin-8 (IL-8), a well-established pulmonary inflammatory cytokine. In primary human macrophages, BP was shown to induce IL-8 expression at both mRNA and secretion levels in a dose-dependent manner. Such an up-regulation was likely linked to aryl hydrocarbon receptor (AhR)-activation since BP-mediated IL-8 induction was reduced after AhR expression knock-down through RNA interference. Moreover, electrophoretic mobility shift assays (EMSAs) and chromatin immunoprecipitation experiments showed BP-triggered binding of AhR to a consensus xenobiotic responsive element (XRE) found in the human IL-8 promoter. Finally, BP administration to mice led to over-expression of keratinocyte chemoattractant (KC), the murine functional homologue of IL-8, in lung. It also triggered the recruitment of neutrophils in bronchoalveolar lavage (BAL) fluids, which was however fully abolished in the presence of a chemical antagonist of the KC/IL-8 receptors CXCR1/CXCR2, thus supporting the functional and crucial involvement of KC in BP-induced lung inflammation. Overall, these data highlight an AhR-dependent regulation of IL-8 in response to BP that likely contributes to the airway inflammatory effects of this environmental chemical.</description><identifier>ISSN: 0378-4274</identifier><identifier>EISSN: 1879-3169</identifier><identifier>DOI: 10.1016/j.toxlet.2008.01.006</identifier><identifier>PMID: 18289803</identifier><identifier>CODEN: TOLED5</identifier><language>eng</language><publisher>Shannon: Elsevier Ireland Ltd</publisher><subject>Animals ; Aryl hydrocarbon receptor ; Benzo(a)pyrene ; Benzo(a)pyrene - toxicity ; Biological and medical sciences ; Bronchoalveolar Lavage Fluid ; Bronchoalveolar Lavage Fluid - immunology ; Cell Movement ; Chemotactic Factors ; Chemotactic Factors - metabolism ; Chromatin Immunoprecipitation ; CXCR2 ; Electrophoretic Mobility Shift Assay ; Environmental Pollutants ; Environmental Pollutants - toxicity ; Humans ; Inflammation ; Interleukin-8 ; Interleukin-8 - genetics ; Interleukin-8 - metabolism ; Keratinocytes ; Keratinocytes - metabolism ; Life Sciences ; Macrophage ; Macrophages ; Macrophages - immunology ; Medical sciences ; Mice ; Mice, Inbred C57BL ; Neutrophils ; Neutrophils - immunology ; Pneumonia ; Pneumonia - chemically induced ; Pneumonia - immunology ; Receptors, Aryl Hydrocarbon ; Receptors, Aryl Hydrocarbon - genetics ; Receptors, Aryl Hydrocarbon - metabolism ; Receptors, Interleukin-8B ; Receptors, Interleukin-8B - metabolism ; Response Elements ; RNA Interference ; Toxicology ; Up-Regulation</subject><ispartof>Toxicology letters, 2008-03, Vol.177 (2), p.130-137</ispartof><rights>2008 Elsevier Ireland Ltd</rights><rights>2008 INIST-CNRS</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c521t-234701f099eac74a1916852cb8ca04662f86b8723fe2c7c965ae73d59bf904e23</citedby><cites>FETCH-LOGICAL-c521t-234701f099eac74a1916852cb8ca04662f86b8723fe2c7c965ae73d59bf904e23</cites><orcidid>0000-0002-2646-671X ; 0000-0002-2015-2779 ; 0000-0002-2638-3180</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0378427408000088$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=20218760$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18289803$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00673238$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Podechard, Normand</creatorcontrib><creatorcontrib>Lecureur, Valérie</creatorcontrib><creatorcontrib>Le Ferrec, Eric</creatorcontrib><creatorcontrib>Guenon, Isabelle</creatorcontrib><creatorcontrib>Sparfel, Lydie</creatorcontrib><creatorcontrib>Gilot, David</creatorcontrib><creatorcontrib>Gordon, John R.</creatorcontrib><creatorcontrib>Lagente, Vincent</creatorcontrib><creatorcontrib>Fardel, Olivier</creatorcontrib><title>Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation</title><title>Toxicology letters</title><addtitle>Toxicol Lett</addtitle><description>Benzo(a)pyrene (BP) is an environmental contaminant known to favor airway inflammation likely through up-regulation of pro-inflammatory cytokines. The present study was designed to characterize its effects toward interleukin-8 (IL-8), a well-established pulmonary inflammatory cytokine. In primary human macrophages, BP was shown to induce IL-8 expression at both mRNA and secretion levels in a dose-dependent manner. Such an up-regulation was likely linked to aryl hydrocarbon receptor (AhR)-activation since BP-mediated IL-8 induction was reduced after AhR expression knock-down through RNA interference. Moreover, electrophoretic mobility shift assays (EMSAs) and chromatin immunoprecipitation experiments showed BP-triggered binding of AhR to a consensus xenobiotic responsive element (XRE) found in the human IL-8 promoter. Finally, BP administration to mice led to over-expression of keratinocyte chemoattractant (KC), the murine functional homologue of IL-8, in lung. It also triggered the recruitment of neutrophils in bronchoalveolar lavage (BAL) fluids, which was however fully abolished in the presence of a chemical antagonist of the KC/IL-8 receptors CXCR1/CXCR2, thus supporting the functional and crucial involvement of KC in BP-induced lung inflammation. Overall, these data highlight an AhR-dependent regulation of IL-8 in response to BP that likely contributes to the airway inflammatory effects of this environmental chemical.</description><subject>Animals</subject><subject>Aryl hydrocarbon receptor</subject><subject>Benzo(a)pyrene</subject><subject>Benzo(a)pyrene - toxicity</subject><subject>Biological and medical sciences</subject><subject>Bronchoalveolar Lavage Fluid</subject><subject>Bronchoalveolar Lavage Fluid - immunology</subject><subject>Cell Movement</subject><subject>Chemotactic Factors</subject><subject>Chemotactic Factors - metabolism</subject><subject>Chromatin Immunoprecipitation</subject><subject>CXCR2</subject><subject>Electrophoretic Mobility Shift Assay</subject><subject>Environmental Pollutants</subject><subject>Environmental Pollutants - toxicity</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Interleukin-8</subject><subject>Interleukin-8 - genetics</subject><subject>Interleukin-8 - metabolism</subject><subject>Keratinocytes</subject><subject>Keratinocytes - metabolism</subject><subject>Life Sciences</subject><subject>Macrophage</subject><subject>Macrophages</subject><subject>Macrophages - immunology</subject><subject>Medical sciences</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neutrophils</subject><subject>Neutrophils - immunology</subject><subject>Pneumonia</subject><subject>Pneumonia - chemically induced</subject><subject>Pneumonia - immunology</subject><subject>Receptors, Aryl Hydrocarbon</subject><subject>Receptors, Aryl Hydrocarbon - genetics</subject><subject>Receptors, Aryl Hydrocarbon - metabolism</subject><subject>Receptors, Interleukin-8B</subject><subject>Receptors, Interleukin-8B - metabolism</subject><subject>Response Elements</subject><subject>RNA Interference</subject><subject>Toxicology</subject><subject>Up-Regulation</subject><issn>0378-4274</issn><issn>1879-3169</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kcFu1DAQhiMEotvCGyDkC6g9JNhO4tiXSlUFtNJKXOBsOc6E9eLYi-2sWN6Bd8ZRVuXGaaTRN_-M5iuKNwRXBBP2YV8l_8tCqijGvMKkwpg9KzaEd6KsCRPPiw2uO142tGsuissY9zgTDWtfFheEUy44rjfFn0eXIFiYfxhXcmTcMOtkvEP9CaUdIHBHE7ybwCVlkfa5TMYpl1AP7re_VjeHUwAHyESkwsmi3WkIXqvQ54wAGg7Jh3KAA7ghZyDlBmRBDRElj-zsvueVo1XTpJatr4oXo7IRXp_rVfHt08ev9w_l9svnx_u7balbSlJJ66bDZMRCgNJdo4ggjLdU91wr3DBGR8563tF6BKo7LViroKuHVvSjwA3Q-qq4WXN3yspDMFM-XXpl5MPdVi69_KmupjU_ksy-X9lD8D9niElOJmqwVjnwc5QUtw2nRGSwWUEdfIwBxqdkguWiTO7lqkwuyiQmy5o89vacP_cTDP-Gzo4y8O4MqKiVHYNy2sQnjmKanTOcuduVg_y5o4EgozbgNAwmi0hy8Ob_l_wFx3q4yw</recordid><startdate>20080315</startdate><enddate>20080315</enddate><creator>Podechard, Normand</creator><creator>Lecureur, Valérie</creator><creator>Le Ferrec, Eric</creator><creator>Guenon, Isabelle</creator><creator>Sparfel, Lydie</creator><creator>Gilot, David</creator><creator>Gordon, John R.</creator><creator>Lagente, Vincent</creator><creator>Fardel, Olivier</creator><general>Elsevier Ireland Ltd</general><general>Elsevier Science</general><general>Elsevier</general><scope>IQODW</scope><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>7T5</scope><scope>7U7</scope><scope>C1K</scope><scope>H94</scope><scope>1XC</scope><orcidid>https://orcid.org/0000-0002-2646-671X</orcidid><orcidid>https://orcid.org/0000-0002-2015-2779</orcidid><orcidid>https://orcid.org/0000-0002-2638-3180</orcidid></search><sort><creationdate>20080315</creationdate><title>Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation</title><author>Podechard, Normand ; Lecureur, Valérie ; Le Ferrec, Eric ; Guenon, Isabelle ; Sparfel, Lydie ; Gilot, David ; Gordon, John R. ; Lagente, Vincent ; Fardel, Olivier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c521t-234701f099eac74a1916852cb8ca04662f86b8723fe2c7c965ae73d59bf904e23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Animals</topic><topic>Aryl hydrocarbon receptor</topic><topic>Benzo(a)pyrene</topic><topic>Benzo(a)pyrene - toxicity</topic><topic>Biological and medical sciences</topic><topic>Bronchoalveolar Lavage Fluid</topic><topic>Bronchoalveolar Lavage Fluid - immunology</topic><topic>Cell Movement</topic><topic>Chemotactic Factors</topic><topic>Chemotactic Factors - metabolism</topic><topic>Chromatin Immunoprecipitation</topic><topic>CXCR2</topic><topic>Electrophoretic Mobility Shift Assay</topic><topic>Environmental Pollutants</topic><topic>Environmental Pollutants - toxicity</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Interleukin-8</topic><topic>Interleukin-8 - genetics</topic><topic>Interleukin-8 - metabolism</topic><topic>Keratinocytes</topic><topic>Keratinocytes - metabolism</topic><topic>Life Sciences</topic><topic>Macrophage</topic><topic>Macrophages</topic><topic>Macrophages - immunology</topic><topic>Medical sciences</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neutrophils</topic><topic>Neutrophils - immunology</topic><topic>Pneumonia</topic><topic>Pneumonia - chemically induced</topic><topic>Pneumonia - immunology</topic><topic>Receptors, Aryl Hydrocarbon</topic><topic>Receptors, Aryl Hydrocarbon - genetics</topic><topic>Receptors, Aryl Hydrocarbon - metabolism</topic><topic>Receptors, Interleukin-8B</topic><topic>Receptors, Interleukin-8B - metabolism</topic><topic>Response Elements</topic><topic>RNA Interference</topic><topic>Toxicology</topic><topic>Up-Regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Podechard, Normand</creatorcontrib><creatorcontrib>Lecureur, Valérie</creatorcontrib><creatorcontrib>Le Ferrec, Eric</creatorcontrib><creatorcontrib>Guenon, Isabelle</creatorcontrib><creatorcontrib>Sparfel, Lydie</creatorcontrib><creatorcontrib>Gilot, David</creatorcontrib><creatorcontrib>Gordon, John R.</creatorcontrib><creatorcontrib>Lagente, Vincent</creatorcontrib><creatorcontrib>Fardel, Olivier</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Toxicology letters</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Podechard, Normand</au><au>Lecureur, Valérie</au><au>Le Ferrec, Eric</au><au>Guenon, Isabelle</au><au>Sparfel, Lydie</au><au>Gilot, David</au><au>Gordon, John R.</au><au>Lagente, Vincent</au><au>Fardel, Olivier</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation</atitle><jtitle>Toxicology letters</jtitle><addtitle>Toxicol Lett</addtitle><date>2008-03-15</date><risdate>2008</risdate><volume>177</volume><issue>2</issue><spage>130</spage><epage>137</epage><pages>130-137</pages><issn>0378-4274</issn><eissn>1879-3169</eissn><coden>TOLED5</coden><abstract>Benzo(a)pyrene (BP) is an environmental contaminant known to favor airway inflammation likely through up-regulation of pro-inflammatory cytokines. The present study was designed to characterize its effects toward interleukin-8 (IL-8), a well-established pulmonary inflammatory cytokine. In primary human macrophages, BP was shown to induce IL-8 expression at both mRNA and secretion levels in a dose-dependent manner. Such an up-regulation was likely linked to aryl hydrocarbon receptor (AhR)-activation since BP-mediated IL-8 induction was reduced after AhR expression knock-down through RNA interference. Moreover, electrophoretic mobility shift assays (EMSAs) and chromatin immunoprecipitation experiments showed BP-triggered binding of AhR to a consensus xenobiotic responsive element (XRE) found in the human IL-8 promoter. Finally, BP administration to mice led to over-expression of keratinocyte chemoattractant (KC), the murine functional homologue of IL-8, in lung. It also triggered the recruitment of neutrophils in bronchoalveolar lavage (BAL) fluids, which was however fully abolished in the presence of a chemical antagonist of the KC/IL-8 receptors CXCR1/CXCR2, thus supporting the functional and crucial involvement of KC in BP-induced lung inflammation. Overall, these data highlight an AhR-dependent regulation of IL-8 in response to BP that likely contributes to the airway inflammatory effects of this environmental chemical.</abstract><cop>Shannon</cop><cop>Amsterdam</cop><pub>Elsevier Ireland Ltd</pub><pmid>18289803</pmid><doi>10.1016/j.toxlet.2008.01.006</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-2646-671X</orcidid><orcidid>https://orcid.org/0000-0002-2015-2779</orcidid><orcidid>https://orcid.org/0000-0002-2638-3180</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0378-4274 |
| ispartof | Toxicology letters, 2008-03, Vol.177 (2), p.130-137 |
| issn | 0378-4274 1879-3169 |
| language | eng |
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| source | MEDLINE; Elsevier ScienceDirect Journals |
| subjects | Animals Aryl hydrocarbon receptor Benzo(a)pyrene Benzo(a)pyrene - toxicity Biological and medical sciences Bronchoalveolar Lavage Fluid Bronchoalveolar Lavage Fluid - immunology Cell Movement Chemotactic Factors Chemotactic Factors - metabolism Chromatin Immunoprecipitation CXCR2 Electrophoretic Mobility Shift Assay Environmental Pollutants Environmental Pollutants - toxicity Humans Inflammation Interleukin-8 Interleukin-8 - genetics Interleukin-8 - metabolism Keratinocytes Keratinocytes - metabolism Life Sciences Macrophage Macrophages Macrophages - immunology Medical sciences Mice Mice, Inbred C57BL Neutrophils Neutrophils - immunology Pneumonia Pneumonia - chemically induced Pneumonia - immunology Receptors, Aryl Hydrocarbon Receptors, Aryl Hydrocarbon - genetics Receptors, Aryl Hydrocarbon - metabolism Receptors, Interleukin-8B Receptors, Interleukin-8B - metabolism Response Elements RNA Interference Toxicology Up-Regulation |
| title | Interleukin-8 induction by the environmental contaminant benzo(a)pyrene is aryl hydrocarbon receptor-dependent and leads to lung inflammation |
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