Prostaglandin E2                          stimulates adaptive IL-22 production and promotes allergic contact dermatitis

Calum T. Robb; Henry J. McSorley; Jinju Lee; Tomohiro Aoki; Cunjing Yu; Siobhan Crittenden; Anne Astier; Jennifer M. Felton; Nicholas Parkinson; Adane Ayele; Richard M. Breyer; Stephen M. Anderton; Shuh Narumiya; Adriano G. Rossi; Sarah E. Howie; Emma Guttman-Yassky; Richard B. Weller; Chengcan Yao

doi:10.1016/j.jaci.2017.04.045

Prostaglandin E₂ stimulates adaptive IL-22 production and promotes allergic contact dermatitis

Calum T. Robb, Henry J. McSorley, Jinju Lee, Tomohiro Aoki, Cunjing Yu, Siobhan Crittenden, Anne Astier, Jennifer M. Felton, Nicholas Parkinson, Adane Ayele, Richard M. Breyer, Stephen M. Anderton, Shuh Narumiya, Adriano G. Rossi, Sarah E. Howie, Emma Guttman-Yassky, Richard B. Weller, Chengcan Yao

Cell Signalling and Immunology

Research output: Contribution to journal › Article › peer-review

44 Citations (Scopus)

Abstract

Background: Atopic dermatitis (AD) and allergic contact dermatitis (ACD) are both forms of eczema and are common inflammatory skin diseases with a central role of T cell-derived IL-22 in their pathogenesis. Although prostaglandin (PG) E ₂ is known to promote inflammation, little is known about its role in processes related to AD and ACD development, including IL-22 upregulation.

Objectives: We sought to investigate whether PGE ₂ has a role in IL-22 induction and development of ACD, which has increased prevalence in patients with AD.

Methods: T-cell cultures and in vivo sensitization of mice with haptens were used to assess the role of PGE ₂ in IL-22 production. The involvement of PGE ₂ receptors and their downstream signals was also examined. The effects of PGE ₂ were evaluated by using the oxazolone-induced ACD mouse model. The relationship of PGE ₂ and IL-22 signaling pathways in skin inflammation were also investigated by using genomic profiling in human lesional AD skin.

Results: PGE ₂ induces IL-22 from T cells through its receptors, E prostanoid receptor (EP) 2 and EP4, and involves cyclic AMP signaling. Selective deletion of EP4 in T cells prevents hapten-induced IL-22 production in vivo, and limits atopic-like skin inflammation in the oxazolone-induced ACD model. Moreover, both PGE ₂ and IL-22 pathway genes were coordinately upregulated in human AD lesional skin but were at less than significant detection levels after corticosteroid or UVB treatments.

Conclusions: Our results define a crucial role for PGE ₂ in promoting ACD by facilitating IL-22 production from T cells.

Original language	English
Pages (from-to)	152-162
Number of pages	11
Journal	Journal of Allergy and Clinical Immunology
Volume	141
Issue number	1
Early online date	3 Jun 2017
DOIs	https://doi.org/10.1016/j.jaci.2017.04.045
Publication status	Published - Jan 2018

Keywords

Allergic contact dermatitis
atopic dermatitis
CD4 T cells
IL-22
prostaglandin E
T 17 cells
T 22 cells

ASJC Scopus subject areas

Immunology and Allergy
Immunology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.jaci.2017.04.045Licence: Elsevier User Licence

Cite this

Robb, C. T., McSorley, H. J., Lee, J., Aoki, T., Yu, C., Crittenden, S., Astier, A., Felton, J. M., Parkinson, N., Ayele, A., Breyer, R. M., Anderton, S. M., Narumiya, S., Rossi, A. G., Howie, S. E., Guttman-Yassky, E., Weller, R. B., & Yao, C. (2018). Prostaglandin E₂ stimulates adaptive IL-22 production and promotes allergic contact dermatitis. Journal of Allergy and Clinical Immunology, 141(1), 152-162. https://doi.org/10.1016/j.jaci.2017.04.045

@article{baf294649f89420090c0c1f1127b8c3c,

title = "Prostaglandin E2 stimulates adaptive IL-22 production and promotes allergic contact dermatitis",

abstract = " Background: Atopic dermatitis (AD) and allergic contact dermatitis (ACD) are both forms of eczema and are common inflammatory skin diseases with a central role of T cell-derived IL-22 in their pathogenesis. Although prostaglandin (PG) E 2 is known to promote inflammation, little is known about its role in processes related to AD and ACD development, including IL-22 upregulation.Objectives: We sought to investigate whether PGE 2 has a role in IL-22 induction and development of ACD, which has increased prevalence in patients with AD.Methods: T-cell cultures and in vivo sensitization of mice with haptens were used to assess the role of PGE 2 in IL-22 production. The involvement of PGE 2 receptors and their downstream signals was also examined. The effects of PGE 2 were evaluated by using the oxazolone-induced ACD mouse model. The relationship of PGE 2 and IL-22 signaling pathways in skin inflammation were also investigated by using genomic profiling in human lesional AD skin.Results: PGE 2 induces IL-22 from T cells through its receptors, E prostanoid receptor (EP) 2 and EP4, and involves cyclic AMP signaling. Selective deletion of EP4 in T cells prevents hapten-induced IL-22 production in vivo, and limits atopic-like skin inflammation in the oxazolone-induced ACD model. Moreover, both PGE 2 and IL-22 pathway genes were coordinately upregulated in human AD lesional skin but were at less than significant detection levels after corticosteroid or UVB treatments.Conclusions: Our results define a crucial role for PGE 2 in promoting ACD by facilitating IL-22 production from T cells. ",

keywords = "Allergic contact dermatitis, atopic dermatitis, CD4 T cells, IL-22, prostaglandin E, T 17 cells, T 22 cells",

author = "Robb, {Calum T.} and McSorley, {Henry J.} and Jinju Lee and Tomohiro Aoki and Cunjing Yu and Siobhan Crittenden and Anne Astier and Felton, {Jennifer M.} and Nicholas Parkinson and Adane Ayele and Breyer, {Richard M.} and Anderton, {Stephen M.} and Shuh Narumiya and Rossi, {Adriano G.} and Howie, {Sarah E.} and Emma Guttman-Yassky and Weller, {Richard B.} and Chengcan Yao",

year = "2018",

month = jan,

doi = "10.1016/j.jaci.2017.04.045",

language = "English",

volume = "141",

pages = "152--162",

journal = "Journal of Allergy and Clinical Immunology",

issn = "0091-6749",

publisher = "Elsevier",

number = "1",

}

Robb, CT, McSorley, HJ, Lee, J, Aoki, T, Yu, C, Crittenden, S, Astier, A, Felton, JM, Parkinson, N, Ayele, A, Breyer, RM, Anderton, SM, Narumiya, S, Rossi, AG, Howie, SE, Guttman-Yassky, E, Weller, RB & Yao, C 2018, 'Prostaglandin E₂ stimulates adaptive IL-22 production and promotes allergic contact dermatitis', Journal of Allergy and Clinical Immunology, vol. 141, no. 1, pp. 152-162. https://doi.org/10.1016/j.jaci.2017.04.045

TY - JOUR

T1 - Prostaglandin E2 stimulates adaptive IL-22 production and promotes allergic contact dermatitis

AU - Robb, Calum T.

AU - McSorley, Henry J.

AU - Lee, Jinju

AU - Aoki, Tomohiro

AU - Yu, Cunjing

AU - Crittenden, Siobhan

AU - Astier, Anne

AU - Felton, Jennifer M.

AU - Parkinson, Nicholas

AU - Ayele, Adane

AU - Breyer, Richard M.

AU - Anderton, Stephen M.

AU - Narumiya, Shuh

AU - Rossi, Adriano G.

AU - Howie, Sarah E.

AU - Guttman-Yassky, Emma

AU - Weller, Richard B.

AU - Yao, Chengcan

PY - 2018/1

Y1 - 2018/1

N2 - Background: Atopic dermatitis (AD) and allergic contact dermatitis (ACD) are both forms of eczema and are common inflammatory skin diseases with a central role of T cell-derived IL-22 in their pathogenesis. Although prostaglandin (PG) E 2 is known to promote inflammation, little is known about its role in processes related to AD and ACD development, including IL-22 upregulation.Objectives: We sought to investigate whether PGE 2 has a role in IL-22 induction and development of ACD, which has increased prevalence in patients with AD.Methods: T-cell cultures and in vivo sensitization of mice with haptens were used to assess the role of PGE 2 in IL-22 production. The involvement of PGE 2 receptors and their downstream signals was also examined. The effects of PGE 2 were evaluated by using the oxazolone-induced ACD mouse model. The relationship of PGE 2 and IL-22 signaling pathways in skin inflammation were also investigated by using genomic profiling in human lesional AD skin.Results: PGE 2 induces IL-22 from T cells through its receptors, E prostanoid receptor (EP) 2 and EP4, and involves cyclic AMP signaling. Selective deletion of EP4 in T cells prevents hapten-induced IL-22 production in vivo, and limits atopic-like skin inflammation in the oxazolone-induced ACD model. Moreover, both PGE 2 and IL-22 pathway genes were coordinately upregulated in human AD lesional skin but were at less than significant detection levels after corticosteroid or UVB treatments.Conclusions: Our results define a crucial role for PGE 2 in promoting ACD by facilitating IL-22 production from T cells.

AB - Background: Atopic dermatitis (AD) and allergic contact dermatitis (ACD) are both forms of eczema and are common inflammatory skin diseases with a central role of T cell-derived IL-22 in their pathogenesis. Although prostaglandin (PG) E 2 is known to promote inflammation, little is known about its role in processes related to AD and ACD development, including IL-22 upregulation.Objectives: We sought to investigate whether PGE 2 has a role in IL-22 induction and development of ACD, which has increased prevalence in patients with AD.Methods: T-cell cultures and in vivo sensitization of mice with haptens were used to assess the role of PGE 2 in IL-22 production. The involvement of PGE 2 receptors and their downstream signals was also examined. The effects of PGE 2 were evaluated by using the oxazolone-induced ACD mouse model. The relationship of PGE 2 and IL-22 signaling pathways in skin inflammation were also investigated by using genomic profiling in human lesional AD skin.Results: PGE 2 induces IL-22 from T cells through its receptors, E prostanoid receptor (EP) 2 and EP4, and involves cyclic AMP signaling. Selective deletion of EP4 in T cells prevents hapten-induced IL-22 production in vivo, and limits atopic-like skin inflammation in the oxazolone-induced ACD model. Moreover, both PGE 2 and IL-22 pathway genes were coordinately upregulated in human AD lesional skin but were at less than significant detection levels after corticosteroid or UVB treatments.Conclusions: Our results define a crucial role for PGE 2 in promoting ACD by facilitating IL-22 production from T cells.

KW - Allergic contact dermatitis

KW - atopic dermatitis

KW - CD4 T cells

KW - IL-22

KW - prostaglandin E

KW - T 17 cells

KW - T 22 cells

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DO - 10.1016/j.jaci.2017.04.045

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