IL‐1β induces thymic stromal lymphopoietin and an atopic dermatitis‐like phenotype in reconstructed healthy human epidermis
Atopic dermatitis (AD) is a common skin inflammatory disease characterized by the production of thymic stromal lymphopoietin (TSLP) and marked TH2 polarization. Recent studies suggest that IL‐1β contributes to the development of AD skin inflammation. Here, we have investigated the impact of IL‐1β si...
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Veröffentlicht in: | The Journal of Pathology 2017-06, Vol.242 (2), p.234-245 |
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creator | Bernard, Marine Carrasco, Cédric Laoubi, Léo Guiraud, Béatrice Rozières, Aurore Goujon, Catherine Duplan, Hélène Bessou‐Touya, Sandrine Nicolas, Jean‐François Vocanson, Marc Galliano, Marie‐Florence |
description | Atopic dermatitis (AD) is a common skin inflammatory disease characterized by the production of thymic stromal lymphopoietin (TSLP) and marked TH2 polarization. Recent studies suggest that IL‐1β contributes to the development of AD skin inflammation. Here, we have investigated the impact of IL‐1β signalling on the epidermal homeostasis of both healthy subjects and AD patients [with functional filaggrin (FLG) alleles], with particular attention to TSLP production and keratinocyte differentiation. In healthy reconstructed human epidermis (RHE), IL‐1β promoted (i) robust secretion of TSLP in an NF‐κB‐dependent manner and (ii) a significant decrease in the expression of filaggrin and other proteins of the epidermal differentiation complex. These effects were prevented by treatment of RHE with the anti‐IL‐1β mAb canakinumab and by the IL‐1 receptor antagonist anakinra. Interestingly, RHE generated from AD donors behaved like that of healthy individuals and showed comparable responses to IL‐1β signals. Collectively, our results suggest that IL‐1β may be an early key mediator for the acquisition of an AD phenotype through induction of TSLP and alteration of the epidermal homeostasis. Copyright © 2017 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd. |
doi_str_mv | 10.1002/path.4887 |
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Recent studies suggest that IL‐1β contributes to the development of AD skin inflammation. Here, we have investigated the impact of IL‐1β signalling on the epidermal homeostasis of both healthy subjects and AD patients [with functional filaggrin (FLG) alleles], with particular attention to TSLP production and keratinocyte differentiation. In healthy reconstructed human epidermis (RHE), IL‐1β promoted (i) robust secretion of TSLP in an NF‐κB‐dependent manner and (ii) a significant decrease in the expression of filaggrin and other proteins of the epidermal differentiation complex. These effects were prevented by treatment of RHE with the anti‐IL‐1β mAb canakinumab and by the IL‐1 receptor antagonist anakinra. Interestingly, RHE generated from AD donors behaved like that of healthy individuals and showed comparable responses to IL‐1β signals. Collectively, our results suggest that IL‐1β may be an early key mediator for the acquisition of an AD phenotype through induction of TSLP and alteration of the epidermal homeostasis. Copyright © 2017 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</description><identifier>ISSN: 0022-3417</identifier><identifier>EISSN: 1096-9896</identifier><identifier>DOI: 10.1002/path.4887</identifier><identifier>PMID: 28191908</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Adult ; Antibodies, Monoclonal - therapeutic use ; atopic dermatitis ; Bacteriology ; Cell Differentiation ; Cytokines - genetics ; Cytokines - secretion ; Dermatitis, Atopic - drug therapy ; Dermatitis, Atopic - genetics ; Dermatitis, Atopic - metabolism ; Dermatitis, Atopic - pathology ; Epidermis - metabolism ; Epidermis - pathology ; Female ; filaggrin ; Homeostasis ; Humans ; IL‐1β ; Immunology ; Interleukin 1 Receptor Antagonist Protein - therapeutic use ; Interleukin-1beta - genetics ; Interleukin-1beta - metabolism ; Intermediate Filament Proteins - genetics ; Intermediate Filament Proteins - metabolism ; Life Sciences ; Male ; Microbiology and Parasitology ; Middle Aged ; NF-kappa B - genetics ; NF-kappa B - metabolism ; Phenotype ; reconstructed human epidermis ; TSLP ; Virology ; Young Adult</subject><ispartof>The Journal of Pathology, 2017-06, Vol.242 (2), p.234-245</ispartof><rights>Copyright © 2017 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3597-e5323f021cbfe350ec0535c997f2fe245683e1896bf5f5481bed9427ebc4da153</citedby><cites>FETCH-LOGICAL-c3597-e5323f021cbfe350ec0535c997f2fe245683e1896bf5f5481bed9427ebc4da153</cites><orcidid>0000-0002-3342-2184 ; 0000-0002-0181-8862 ; 0000-0003-4204-803X</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%2Fpath.4887$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fpath.4887$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,886,1418,27929,27930,45579,45580</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28191908$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01911419$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bernard, Marine</creatorcontrib><creatorcontrib>Carrasco, Cédric</creatorcontrib><creatorcontrib>Laoubi, Léo</creatorcontrib><creatorcontrib>Guiraud, Béatrice</creatorcontrib><creatorcontrib>Rozières, Aurore</creatorcontrib><creatorcontrib>Goujon, Catherine</creatorcontrib><creatorcontrib>Duplan, Hélène</creatorcontrib><creatorcontrib>Bessou‐Touya, Sandrine</creatorcontrib><creatorcontrib>Nicolas, Jean‐François</creatorcontrib><creatorcontrib>Vocanson, Marc</creatorcontrib><creatorcontrib>Galliano, Marie‐Florence</creatorcontrib><title>IL‐1β induces thymic stromal lymphopoietin and an atopic dermatitis‐like phenotype in reconstructed healthy human epidermis</title><title>The Journal of Pathology</title><addtitle>J Pathol</addtitle><description>Atopic dermatitis (AD) is a common skin inflammatory disease characterized by the production of thymic stromal lymphopoietin (TSLP) and marked TH2 polarization. Recent studies suggest that IL‐1β contributes to the development of AD skin inflammation. Here, we have investigated the impact of IL‐1β signalling on the epidermal homeostasis of both healthy subjects and AD patients [with functional filaggrin (FLG) alleles], with particular attention to TSLP production and keratinocyte differentiation. In healthy reconstructed human epidermis (RHE), IL‐1β promoted (i) robust secretion of TSLP in an NF‐κB‐dependent manner and (ii) a significant decrease in the expression of filaggrin and other proteins of the epidermal differentiation complex. These effects were prevented by treatment of RHE with the anti‐IL‐1β mAb canakinumab and by the IL‐1 receptor antagonist anakinra. Interestingly, RHE generated from AD donors behaved like that of healthy individuals and showed comparable responses to IL‐1β signals. Collectively, our results suggest that IL‐1β may be an early key mediator for the acquisition of an AD phenotype through induction of TSLP and alteration of the epidermal homeostasis. Copyright © 2017 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</description><subject>Adult</subject><subject>Antibodies, Monoclonal - therapeutic use</subject><subject>atopic dermatitis</subject><subject>Bacteriology</subject><subject>Cell Differentiation</subject><subject>Cytokines - genetics</subject><subject>Cytokines - secretion</subject><subject>Dermatitis, Atopic - drug therapy</subject><subject>Dermatitis, Atopic - genetics</subject><subject>Dermatitis, Atopic - metabolism</subject><subject>Dermatitis, Atopic - pathology</subject><subject>Epidermis - metabolism</subject><subject>Epidermis - pathology</subject><subject>Female</subject><subject>filaggrin</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>IL‐1β</subject><subject>Immunology</subject><subject>Interleukin 1 Receptor Antagonist Protein - therapeutic use</subject><subject>Interleukin-1beta - genetics</subject><subject>Interleukin-1beta - metabolism</subject><subject>Intermediate Filament Proteins - genetics</subject><subject>Intermediate Filament Proteins - metabolism</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Microbiology and Parasitology</subject><subject>Middle Aged</subject><subject>NF-kappa B - genetics</subject><subject>NF-kappa B - metabolism</subject><subject>Phenotype</subject><subject>reconstructed human epidermis</subject><subject>TSLP</subject><subject>Virology</subject><subject>Young Adult</subject><issn>0022-3417</issn><issn>1096-9896</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUFu1DAUhi1ERYeWBRdAXsIire3EE3s5qoCpNBIs2rXlOC-KwYlN7FBl1yNwFg7CITgJDlPKqosnS8-fP73nH6HXlFxQQthl0Km_qISon6ENJXJbSCG3z9Em37GirGh9il7G-IUQIiXnL9ApE1RSScQG3V8fft__oL9-Yju2s4GIU78M1uCYJj9oh90yhN4HbyHZEeuxzYV18iEzLUyDTjbZmB3OfgUcehh9WgJkHZ7A-DF7ZpOgxT1ol924n4dsgGDX1zaeo5NOuwivHs4zdPvh_c3Vvjh8-nh9tTsUpuSyLoCXrOwIo6bpoOQEDOElN1LWHeuAVXwrSqB57abjHa8EbaCVFauhMVWrKS_P0Lujt9dOhckOelqU11btdwe19kj-ElpR-Z1m9u2RDZP_NkNMKg9qwDk9gp-jomJbS1ExWv_XmsnHOEH36KZEreGoNRy1hpPZNw_auRmgfST_pZGByyNwZx0sT5vU593N_q_yDwL9niY</recordid><startdate>201706</startdate><enddate>201706</enddate><creator>Bernard, Marine</creator><creator>Carrasco, Cédric</creator><creator>Laoubi, Léo</creator><creator>Guiraud, Béatrice</creator><creator>Rozières, Aurore</creator><creator>Goujon, Catherine</creator><creator>Duplan, Hélène</creator><creator>Bessou‐Touya, Sandrine</creator><creator>Nicolas, Jean‐François</creator><creator>Vocanson, Marc</creator><creator>Galliano, Marie‐Florence</creator><general>John Wiley & Sons, Ltd</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>1XC</scope><orcidid>https://orcid.org/0000-0002-3342-2184</orcidid><orcidid>https://orcid.org/0000-0002-0181-8862</orcidid><orcidid>https://orcid.org/0000-0003-4204-803X</orcidid></search><sort><creationdate>201706</creationdate><title>IL‐1β induces thymic stromal lymphopoietin and an atopic dermatitis‐like phenotype in reconstructed healthy human epidermis</title><author>Bernard, Marine ; Carrasco, Cédric ; Laoubi, Léo ; Guiraud, Béatrice ; Rozières, Aurore ; Goujon, Catherine ; Duplan, Hélène ; Bessou‐Touya, Sandrine ; Nicolas, Jean‐François ; Vocanson, Marc ; Galliano, Marie‐Florence</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3597-e5323f021cbfe350ec0535c997f2fe245683e1896bf5f5481bed9427ebc4da153</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adult</topic><topic>Antibodies, Monoclonal - therapeutic use</topic><topic>atopic dermatitis</topic><topic>Bacteriology</topic><topic>Cell Differentiation</topic><topic>Cytokines - genetics</topic><topic>Cytokines - secretion</topic><topic>Dermatitis, Atopic - drug therapy</topic><topic>Dermatitis, Atopic - genetics</topic><topic>Dermatitis, Atopic - metabolism</topic><topic>Dermatitis, Atopic - pathology</topic><topic>Epidermis - metabolism</topic><topic>Epidermis - pathology</topic><topic>Female</topic><topic>filaggrin</topic><topic>Homeostasis</topic><topic>Humans</topic><topic>IL‐1β</topic><topic>Immunology</topic><topic>Interleukin 1 Receptor Antagonist Protein - therapeutic use</topic><topic>Interleukin-1beta - genetics</topic><topic>Interleukin-1beta - metabolism</topic><topic>Intermediate Filament Proteins - genetics</topic><topic>Intermediate Filament Proteins - metabolism</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Microbiology and Parasitology</topic><topic>Middle Aged</topic><topic>NF-kappa B - genetics</topic><topic>NF-kappa B - metabolism</topic><topic>Phenotype</topic><topic>reconstructed human epidermis</topic><topic>TSLP</topic><topic>Virology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bernard, Marine</creatorcontrib><creatorcontrib>Carrasco, Cédric</creatorcontrib><creatorcontrib>Laoubi, Léo</creatorcontrib><creatorcontrib>Guiraud, Béatrice</creatorcontrib><creatorcontrib>Rozières, Aurore</creatorcontrib><creatorcontrib>Goujon, Catherine</creatorcontrib><creatorcontrib>Duplan, Hélène</creatorcontrib><creatorcontrib>Bessou‐Touya, Sandrine</creatorcontrib><creatorcontrib>Nicolas, Jean‐François</creatorcontrib><creatorcontrib>Vocanson, Marc</creatorcontrib><creatorcontrib>Galliano, Marie‐Florence</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>Hyper Article en Ligne (HAL)</collection><jtitle>The Journal of Pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bernard, Marine</au><au>Carrasco, Cédric</au><au>Laoubi, Léo</au><au>Guiraud, Béatrice</au><au>Rozières, Aurore</au><au>Goujon, Catherine</au><au>Duplan, Hélène</au><au>Bessou‐Touya, Sandrine</au><au>Nicolas, Jean‐François</au><au>Vocanson, Marc</au><au>Galliano, Marie‐Florence</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>IL‐1β induces thymic stromal lymphopoietin and an atopic dermatitis‐like phenotype in reconstructed healthy human epidermis</atitle><jtitle>The Journal of Pathology</jtitle><addtitle>J Pathol</addtitle><date>2017-06</date><risdate>2017</risdate><volume>242</volume><issue>2</issue><spage>234</spage><epage>245</epage><pages>234-245</pages><issn>0022-3417</issn><eissn>1096-9896</eissn><abstract>Atopic dermatitis (AD) is a common skin inflammatory disease characterized by the production of thymic stromal lymphopoietin (TSLP) and marked TH2 polarization. Recent studies suggest that IL‐1β contributes to the development of AD skin inflammation. Here, we have investigated the impact of IL‐1β signalling on the epidermal homeostasis of both healthy subjects and AD patients [with functional filaggrin (FLG) alleles], with particular attention to TSLP production and keratinocyte differentiation. In healthy reconstructed human epidermis (RHE), IL‐1β promoted (i) robust secretion of TSLP in an NF‐κB‐dependent manner and (ii) a significant decrease in the expression of filaggrin and other proteins of the epidermal differentiation complex. These effects were prevented by treatment of RHE with the anti‐IL‐1β mAb canakinumab and by the IL‐1 receptor antagonist anakinra. Interestingly, RHE generated from AD donors behaved like that of healthy individuals and showed comparable responses to IL‐1β signals. Collectively, our results suggest that IL‐1β may be an early key mediator for the acquisition of an AD phenotype through induction of TSLP and alteration of the epidermal homeostasis. Copyright © 2017 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>28191908</pmid><doi>10.1002/path.4887</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-3342-2184</orcidid><orcidid>https://orcid.org/0000-0002-0181-8862</orcidid><orcidid>https://orcid.org/0000-0003-4204-803X</orcidid></addata></record> |
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subjects | Adult Antibodies, Monoclonal - therapeutic use atopic dermatitis Bacteriology Cell Differentiation Cytokines - genetics Cytokines - secretion Dermatitis, Atopic - drug therapy Dermatitis, Atopic - genetics Dermatitis, Atopic - metabolism Dermatitis, Atopic - pathology Epidermis - metabolism Epidermis - pathology Female filaggrin Homeostasis Humans IL‐1β Immunology Interleukin 1 Receptor Antagonist Protein - therapeutic use Interleukin-1beta - genetics Interleukin-1beta - metabolism Intermediate Filament Proteins - genetics Intermediate Filament Proteins - metabolism Life Sciences Male Microbiology and Parasitology Middle Aged NF-kappa B - genetics NF-kappa B - metabolism Phenotype reconstructed human epidermis TSLP Virology Young Adult |
title | IL‐1β induces thymic stromal lymphopoietin and an atopic dermatitis‐like phenotype in reconstructed healthy human epidermis |
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