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

Xiaojie Cai, Maoying Han, Fangzhou Lou, Yang Sun, Qianqian Yin, Libo Sun, Zhikai Wang, Xiangxiao Li, Hong Zhou, Zhenyao Xu, Hong Wang, Siyu Deng, Xichen Zheng, Taiyu Zhang, Qun Li, Bin Zhou () and Honglin Wang ()
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Xiaojie Cai: Shanghai Jiao Tong University School of Medicine
Maoying Han: University of Chinese Academy of Sciences
Fangzhou Lou: Shanghai Jiao Tong University School of Medicine
Yang Sun: Shanghai Jiao Tong University School of Medicine
Qianqian Yin: Shanghai Jiao Tong University School of Medicine
Libo Sun: Shanghai Jiao Tong University School of Medicine
Zhikai Wang: Shanghai Jiao Tong University School of Medicine
Xiangxiao Li: Shanghai Jiao Tong University School of Medicine
Hong Zhou: Shanghai Jiao Tong University School of Medicine
Zhenyao Xu: Shanghai Jiao Tong University School of Medicine
Hong Wang: Shanghai Jiao Tong University School of Medicine
Siyu Deng: Shanghai Jiao Tong University School of Medicine
Xichen Zheng: Shanghai Jiao Tong University School of Medicine
Taiyu Zhang: Shanghai Jiao Tong University School of Medicine
Qun Li: Shanghai Jiao Tong University School of Medicine
Bin Zhou: University of Chinese Academy of Sciences
Honglin Wang: Shanghai Jiao Tong University School of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41467-023-37798-x

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