Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway

Chronic itch is a common and complex symptom often associated with skin diseases such as atopic dermatitis (AD). Although IL-27 is linked to AD, its role and clinical significance in itch remain undefined. We sought to investigate IL-27 function in itch using tissue-specific transgenic mice, various...

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Main Author: Yanqing, Li (author)
Other Authors: Chen, Weiwei (author), Zhu, Xingyun (author), Mei, Huiyuan (author), Steinhoff, Martin (author), Buddenkotte, Joerg (author), Wang, Jinhai (author), Zhang, Wenhao (author), Li, Zhenghui (author), Dai, Xiaolong (author), Shan, Chunxu (author), Wang, Jiafu (author), Meng, Jianghui (author)
Format: article
Published: 2024
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Online Access:http://dx.doi.org/10.1016/j.jid.2024.01.025
https://www.sciencedirect.com/science/article/pii/S0022202X24001088
http://hdl.handle.net/10576/61709
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_version_ 1857415087494529024
author Yanqing, Li
author2 Chen, Weiwei
Zhu, Xingyun
Mei, Huiyuan
Steinhoff, Martin
Buddenkotte, Joerg
Wang, Jinhai
Zhang, Wenhao
Li, Zhenghui
Dai, Xiaolong
Shan, Chunxu
Wang, Jiafu
Meng, Jianghui
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author_facet Yanqing, Li
Chen, Weiwei
Zhu, Xingyun
Mei, Huiyuan
Steinhoff, Martin
Buddenkotte, Joerg
Wang, Jinhai
Zhang, Wenhao
Li, Zhenghui
Dai, Xiaolong
Shan, Chunxu
Wang, Jiafu
Meng, Jianghui
author_role author
dc.creator.none.fl_str_mv Yanqing, Li
Chen, Weiwei
Zhu, Xingyun
Mei, Huiyuan
Steinhoff, Martin
Buddenkotte, Joerg
Wang, Jinhai
Zhang, Wenhao
Li, Zhenghui
Dai, Xiaolong
Shan, Chunxu
Wang, Jiafu
Meng, Jianghui
dc.date.none.fl_str_mv 2024-12-08T08:49:15Z
2024-08-31
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://dx.doi.org/10.1016/j.jid.2024.01.025
Li, Y., Chen, W., Zhu, X., Mei, H., Steinhoff, M., Buddenkotte, J., ... & Meng, J. (2024). Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway. Journal of Investigative Dermatology.
0022-202X
https://www.sciencedirect.com/science/article/pii/S0022202X24001088
http://hdl.handle.net/10576/61709
8
144
1523-1747
dc.language.none.fl_str_mv en
dc.publisher.none.fl_str_mv Elsevier
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Atopic dermatitis
BST2
IL-27
itch
PAR2
dc.title.none.fl_str_mv Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
dc.type.none.fl_str_mv Article
info:eu-repo/semantics/publishedVersion
info:eu-repo/semantics/article
description Chronic itch is a common and complex symptom often associated with skin diseases such as atopic dermatitis (AD). Although IL-27 is linked to AD, its role and clinical significance in itch remain undefined. We sought to investigate IL-27 function in itch using tissue-specific transgenic mice, various itch models, behavior scoring, RNA sequencing, and cytokine/kinase array. Our findings show that IL-27 receptors were overexpressed in human AD skin. Intradermal IL-27 injection failed to directly induce itch in mice but upregulated skin protease-activated receptor 2 (PAR2) transcripts, a key factor in itch and AD. IL-27 activated human keratinocytes, increasing PAR2 transcription and activity. Coinjection of SLIGRL (PAR2 agonist) and IL-27 in mice heightened PAR2-mediated itch. In addition, IL-27 boosted BST2 transcription in sensory neurons and keratinocytes. BST2 was upregulated in AD skin, and its injection in mice induced itch-like response. BST2 colocalized with sensory nerve branches in AD skin from both human and murine models. Sensory neurons released BST2, and mice with sensory neuron–specific BST2 knockout displayed reduced itch responses. Overall, this study provides evidence that skin IL-27/PAR2 and neuronal IL-27/BST2 axes are implicated in cutaneous inflammation and pruritus. The discovery of neuronal BST2 in pruritus shed light on BST2 in the itch cascade.
eu_rights_str_mv openAccess
format article
id qu_181a0ee6252ab4a3cfa37b4b4880a8ab
identifier_str_mv Li, Y., Chen, W., Zhu, X., Mei, H., Steinhoff, M., Buddenkotte, J., ... & Meng, J. (2024). Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway. Journal of Investigative Dermatology.
0022-202X
8
144
1523-1747
language_invalid_str_mv en
network_acronym_str qu
network_name_str Qatar University repository
oai_identifier_str oai:qspace.qu.edu.qa:10576/61709
publishDate 2024
publisher.none.fl_str_mv Elsevier
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repository.name.fl_str_mv
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rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
spelling Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch PathwayYanqing, LiChen, WeiweiZhu, XingyunMei, HuiyuanSteinhoff, MartinBuddenkotte, JoergWang, JinhaiZhang, WenhaoLi, ZhenghuiDai, XiaolongShan, ChunxuWang, JiafuMeng, JianghuiAtopic dermatitisBST2IL-27itchPAR2Chronic itch is a common and complex symptom often associated with skin diseases such as atopic dermatitis (AD). Although IL-27 is linked to AD, its role and clinical significance in itch remain undefined. We sought to investigate IL-27 function in itch using tissue-specific transgenic mice, various itch models, behavior scoring, RNA sequencing, and cytokine/kinase array. Our findings show that IL-27 receptors were overexpressed in human AD skin. Intradermal IL-27 injection failed to directly induce itch in mice but upregulated skin protease-activated receptor 2 (PAR2) transcripts, a key factor in itch and AD. IL-27 activated human keratinocytes, increasing PAR2 transcription and activity. Coinjection of SLIGRL (PAR2 agonist) and IL-27 in mice heightened PAR2-mediated itch. In addition, IL-27 boosted BST2 transcription in sensory neurons and keratinocytes. BST2 was upregulated in AD skin, and its injection in mice induced itch-like response. BST2 colocalized with sensory nerve branches in AD skin from both human and murine models. Sensory neurons released BST2, and mice with sensory neuron–specific BST2 knockout displayed reduced itch responses. Overall, this study provides evidence that skin IL-27/PAR2 and neuronal IL-27/BST2 axes are implicated in cutaneous inflammation and pruritus. The discovery of neuronal BST2 in pruritus shed light on BST2 in the itch cascade.This worked is supported by a fund from National Natural Science of Foundation of China (NSFC 82273509), and a fund from LEO Foundation. It is also funded by National Priorities Research Program (NPRP11S-0117-180326) of the Qatar National Research Fund, Qatar Foundation; and Internal Research Grand Competition (IRGC-04-SI-17-151), MRC Fund, Hamad Medical Corporation, Qatar.Elsevier2024-12-08T08:49:15Z2024-08-31Articleinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://dx.doi.org/10.1016/j.jid.2024.01.025Li, Y., Chen, W., Zhu, X., Mei, H., Steinhoff, M., Buddenkotte, J., ... & Meng, J. (2024). Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway. Journal of Investigative Dermatology.0022-202Xhttps://www.sciencedirect.com/science/article/pii/S0022202X24001088http://hdl.handle.net/10576/6170981441523-1747enhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:qspace.qu.edu.qa:10576/617092024-12-08T19:05:28Z
spellingShingle Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
Yanqing, Li
Atopic dermatitis
BST2
IL-27
itch
PAR2
status_str publishedVersion
title Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
title_full Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
title_fullStr Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
title_full_unstemmed Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
title_short Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
title_sort Neuronal BST2: A Pruritic Mediator alongside Protease-Activated Receptor 2 in the IL-27–Driven Itch Pathway
topic Atopic dermatitis
BST2
IL-27
itch
PAR2
url http://dx.doi.org/10.1016/j.jid.2024.01.025
https://www.sciencedirect.com/science/article/pii/S0022202X24001088
http://hdl.handle.net/10576/61709