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Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis

Dermal fibroblasts and cutaneous nerves are important players in skin diseases, while their reciprocal roles during skin inflammation have not been characterized. Here we identify an inflammation-induced subset of papillary fibroblasts that promotes aberrant neurite outgrowth and psoriasiform skin i...

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Autores principales: Cai, Xiaojie, Han, Maoying, Lou, Fangzhou, Sun, Yang, Yin, Qianqian, Sun, Libo, Wang, Zhikai, Li, Xiangxiao, Zhou, Hong, Xu, Zhenyao, Wang, Hong, Deng, Siyu, Zheng, Xichen, Zhang, Taiyu, Li, Qun, Zhou, Bin, Wang, Honglin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086024/
https://www.ncbi.nlm.nih.gov/pubmed/37037861
http://dx.doi.org/10.1038/s41467-023-37798-x
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author Cai, Xiaojie
Han, Maoying
Lou, Fangzhou
Sun, Yang
Yin, Qianqian
Sun, Libo
Wang, Zhikai
Li, Xiangxiao
Zhou, Hong
Xu, Zhenyao
Wang, Hong
Deng, Siyu
Zheng, Xichen
Zhang, Taiyu
Li, Qun
Zhou, Bin
Wang, Honglin
author_facet Cai, Xiaojie
Han, Maoying
Lou, Fangzhou
Sun, Yang
Yin, Qianqian
Sun, Libo
Wang, Zhikai
Li, Xiangxiao
Zhou, Hong
Xu, Zhenyao
Wang, Hong
Deng, Siyu
Zheng, Xichen
Zhang, Taiyu
Li, Qun
Zhou, Bin
Wang, Honglin
author_sort Cai, Xiaojie
collection PubMed
description Dermal fibroblasts and cutaneous nerves are important players in skin diseases, while their reciprocal roles during skin inflammation have not been characterized. Here we identify an inflammation-induced subset of papillary fibroblasts that promotes aberrant neurite outgrowth and psoriasiform skin inflammation by secreting the extracellular matrix protein tenascin-C (TNC). Single-cell analysis of fibroblast lineages reveals a Tnc(+) papillary fibroblast subset with pro-axonogenesis and neuro-regulation transcriptomic hallmarks. TNC overexpression in fibroblasts boosts neurite outgrowth in co-cultured neurons, while fibroblast-specific TNC ablation suppresses hyperinnervation and alleviates skin inflammation in male mice modeling psoriasis. Dermal γδT cells, the main producers of type 17 pathogenic cytokines, frequently contact nerve fibers in mouse psoriasiform lesions and are likely modulated by postsynaptic signals. Overall, our results highlight the role of an inflammation-responsive fibroblast subset in facilitating neuro-immune synapse formation and suggest potential avenues for future therapeutic research.
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spelling pubmed-100860242023-04-12 Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis Cai, Xiaojie Han, Maoying Lou, Fangzhou Sun, Yang Yin, Qianqian Sun, Libo Wang, Zhikai Li, Xiangxiao Zhou, Hong Xu, Zhenyao Wang, Hong Deng, Siyu Zheng, Xichen Zhang, Taiyu Li, Qun Zhou, Bin Wang, Honglin Nat Commun Article Dermal fibroblasts and cutaneous nerves are important players in skin diseases, while their reciprocal roles during skin inflammation have not been characterized. Here we identify an inflammation-induced subset of papillary fibroblasts that promotes aberrant neurite outgrowth and psoriasiform skin inflammation by secreting the extracellular matrix protein tenascin-C (TNC). Single-cell analysis of fibroblast lineages reveals a Tnc(+) papillary fibroblast subset with pro-axonogenesis and neuro-regulation transcriptomic hallmarks. TNC overexpression in fibroblasts boosts neurite outgrowth in co-cultured neurons, while fibroblast-specific TNC ablation suppresses hyperinnervation and alleviates skin inflammation in male mice modeling psoriasis. Dermal γδT cells, the main producers of type 17 pathogenic cytokines, frequently contact nerve fibers in mouse psoriasiform lesions and are likely modulated by postsynaptic signals. Overall, our results highlight the role of an inflammation-responsive fibroblast subset in facilitating neuro-immune synapse formation and suggest potential avenues for future therapeutic research. Nature Publishing Group UK 2023-04-10 /pmc/articles/PMC10086024/ /pubmed/37037861 http://dx.doi.org/10.1038/s41467-023-37798-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Cai, Xiaojie
Han, Maoying
Lou, Fangzhou
Sun, Yang
Yin, Qianqian
Sun, Libo
Wang, Zhikai
Li, Xiangxiao
Zhou, Hong
Xu, Zhenyao
Wang, Hong
Deng, Siyu
Zheng, Xichen
Zhang, Taiyu
Li, Qun
Zhou, Bin
Wang, Honglin
Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
title Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
title_full Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
title_fullStr Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
title_full_unstemmed Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
title_short Tenascin C(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
title_sort tenascin c(+) papillary fibroblasts facilitate neuro-immune interaction in a mouse model of psoriasis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10086024/
https://www.ncbi.nlm.nih.gov/pubmed/37037861
http://dx.doi.org/10.1038/s41467-023-37798-x
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