Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.

TNFα overexpression has been associated with several chronic inflammatory diseases, including psoriasis, lichen planus, rheumatoid arthritis, and inflammatory bowel disease. Paradoxically, numerous studies have reported new-onset psoriasis and lichen planus following TNFα antagonist therapy. Here, w...

Full description

Saved in:
Bibliographic Details
Main Authors: Sergio Candel, Sofía de Oliveira, Azucena López-Muñoz, Diana García-Moreno, Raquel Espín-Palazón, Sylwia D Tyrkalska, María L Cayuela, Stephen A Renshaw, Raúl Corbalán-Vélez, Inmaculada Vidal-Abarca, Huai-Jen Tsai, José Meseguer, María P Sepulcre, Victoriano Mulero
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-05-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.1001855
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849332365905625088
author Sergio Candel
Sofía de Oliveira
Azucena López-Muñoz
Diana García-Moreno
Raquel Espín-Palazón
Sylwia D Tyrkalska
María L Cayuela
Stephen A Renshaw
Raúl Corbalán-Vélez
Inmaculada Vidal-Abarca
Huai-Jen Tsai
José Meseguer
María P Sepulcre
Victoriano Mulero
author_facet Sergio Candel
Sofía de Oliveira
Azucena López-Muñoz
Diana García-Moreno
Raquel Espín-Palazón
Sylwia D Tyrkalska
María L Cayuela
Stephen A Renshaw
Raúl Corbalán-Vélez
Inmaculada Vidal-Abarca
Huai-Jen Tsai
José Meseguer
María P Sepulcre
Victoriano Mulero
author_sort Sergio Candel
collection DOAJ
description TNFα overexpression has been associated with several chronic inflammatory diseases, including psoriasis, lichen planus, rheumatoid arthritis, and inflammatory bowel disease. Paradoxically, numerous studies have reported new-onset psoriasis and lichen planus following TNFα antagonist therapy. Here, we show that genetic inhibition of Tnfa and Tnfr2 in zebrafish results in the mobilization of neutrophils to the skin. Using combinations of fluorescent reporter transgenes, fluorescence microscopy, and flow cytometry, we identified the local production of dual oxidase 1 (Duox1)-derived H₂O₂ by Tnfa- and Tnfr2-deficient keratinocytes as a trigger for the activation of the master inflammation transcription factor NF-κB, which then promotes the induction of genes encoding pro-inflammatory molecules. In addition, pharmacological inhibition of Duox1 completely abrogated skin inflammation, placing Duox1-derived H₂O₂ upstream of this positive feedback inflammatory loop. Strikingly, DUOX1 was drastically induced in the skin lesions of psoriasis and lichen planus patients. These results reveal a crucial role for TNFα/TNFR2 axis in the protection of the skin against DUOX1-mediated oxidative stress and could establish new therapeutic targets for skin inflammatory disorders.
format Article
id doaj-art-eff14dad52ab4e5ea1a64dd68ff5a645
institution Kabale University
issn 1544-9173
1545-7885
language English
publishDate 2014-05-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Biology
spelling doaj-art-eff14dad52ab4e5ea1a64dd68ff5a6452025-08-20T03:46:12ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852014-05-01125e100185510.1371/journal.pbio.1001855Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.Sergio CandelSofía de OliveiraAzucena López-MuñozDiana García-MorenoRaquel Espín-PalazónSylwia D TyrkalskaMaría L CayuelaStephen A RenshawRaúl Corbalán-VélezInmaculada Vidal-AbarcaHuai-Jen TsaiJosé MeseguerMaría P SepulcreVictoriano MuleroTNFα overexpression has been associated with several chronic inflammatory diseases, including psoriasis, lichen planus, rheumatoid arthritis, and inflammatory bowel disease. Paradoxically, numerous studies have reported new-onset psoriasis and lichen planus following TNFα antagonist therapy. Here, we show that genetic inhibition of Tnfa and Tnfr2 in zebrafish results in the mobilization of neutrophils to the skin. Using combinations of fluorescent reporter transgenes, fluorescence microscopy, and flow cytometry, we identified the local production of dual oxidase 1 (Duox1)-derived H₂O₂ by Tnfa- and Tnfr2-deficient keratinocytes as a trigger for the activation of the master inflammation transcription factor NF-κB, which then promotes the induction of genes encoding pro-inflammatory molecules. In addition, pharmacological inhibition of Duox1 completely abrogated skin inflammation, placing Duox1-derived H₂O₂ upstream of this positive feedback inflammatory loop. Strikingly, DUOX1 was drastically induced in the skin lesions of psoriasis and lichen planus patients. These results reveal a crucial role for TNFα/TNFR2 axis in the protection of the skin against DUOX1-mediated oxidative stress and could establish new therapeutic targets for skin inflammatory disorders.https://doi.org/10.1371/journal.pbio.1001855
spellingShingle Sergio Candel
Sofía de Oliveira
Azucena López-Muñoz
Diana García-Moreno
Raquel Espín-Palazón
Sylwia D Tyrkalska
María L Cayuela
Stephen A Renshaw
Raúl Corbalán-Vélez
Inmaculada Vidal-Abarca
Huai-Jen Tsai
José Meseguer
María P Sepulcre
Victoriano Mulero
Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.
PLoS Biology
title Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.
title_full Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.
title_fullStr Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.
title_full_unstemmed Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.
title_short Tnfa signaling through tnfr2 protects skin against oxidative stress-induced inflammation.
title_sort tnfa signaling through tnfr2 protects skin against oxidative stress induced inflammation
url https://doi.org/10.1371/journal.pbio.1001855
work_keys_str_mv AT sergiocandel tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT sofiadeoliveira tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT azucenalopezmunoz tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT dianagarciamoreno tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT raquelespinpalazon tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT sylwiadtyrkalska tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT marialcayuela tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT stephenarenshaw tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT raulcorbalanvelez tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT inmaculadavidalabarca tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT huaijentsai tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT josemeseguer tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT mariapsepulcre tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation
AT victorianomulero tnfasignalingthroughtnfr2protectsskinagainstoxidativestressinducedinflammation