Tonic type 2 immunity is a critical tissue checkpoint controlling autoimmunity in the skin
Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid me...
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Published in | Cell reports (Cambridge) Vol. 43; no. 7; p. 114364 |
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Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
23.07.2024
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Abstract | Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid metabolism, as well as Th2 signature. Homeostatic expression of liver X receptor (LXR) and peroxisome proliferator-activated receptor gamma (PPARγ) is essential for maintaining fatty acid metabolism and for conferring resistance to psoriasis in mice. Perturbation of signal transducer and activator of transcription 6 (STAT6) diminishes the homeostatic levels of LXR and PPARγ. Furthermore, mice lacking STAT6, interleukin 4 receptor alpha (IL-4Rα), or IL-13, but not IL-4, exhibit increased susceptibility to psoriasis. Under steady state, innate lymphoid cells (ILCs) are the primary producers of IL-13. In human skin, inhibiting tonic type 2 immunity exacerbates psoriasis-like inflammation and IL-17A, while activating LXR or PPARγ inhibits them. Hence, we propose that tonic type 2 immunity, driven by IL-13-producing ILCs, represents a crucial tissue checkpoint that represses autoimmunity and maintains lipid homeostasis in the skin.
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•Psoriasis induces a downregulation of fatty acid metabolism and Th2 signature genes•LXR and PPARγ are required for the resistance to psoriasis and lipid homeostasis•IL-13-producing ILCs are responsible for tonic type 2 immunity in normal skin•Inhibiting tonic type 2 immunity worsens psoriatic inflammation in mice and humans
Lee et al. show that fatty acid dysregulation occurs in psoriatic skin. Lack of LXR or PPARγ exacerbates psoriasis progression, and LXR and PPARγ homeostasis is maintained by tonic type 2 immunity. IL-13-producing ILCs are in charge of tonic type 2 immunity and contribute to the resistance to autoimmunity. |
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AbstractList | Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid metabolism, as well as Th2 signature. Homeostatic expression of liver X receptor (LXR) and peroxisome proliferator-activated receptor gamma (PPARγ) is essential for maintaining fatty acid metabolism and for conferring resistance to psoriasis in mice. Perturbation of signal transducer and activator of transcription 6 (STAT6) diminishes the homeostatic levels of LXR and PPARγ. Furthermore, mice lacking STAT6, interleukin 4 receptor alpha (IL-4Rα), or IL-13, but not IL-4, exhibit increased susceptibility to psoriasis. Under steady state, innate lymphoid cells (ILCs) are the primary producers of IL-13. In human skin, inhibiting tonic type 2 immunity exacerbates psoriasis-like inflammation and IL-17A, while activating LXR or PPARγ inhibits them. Hence, we propose that tonic type 2 immunity, driven by IL-13-producing ILCs, represents a crucial tissue checkpoint that represses autoimmunity and maintains lipid homeostasis in the skin. Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid metabolism, as well as Th2 signature. Homeostatic expression of liver X receptor (LXR) and peroxisome proliferator-activated receptor gamma (PPARγ) is essential for maintaining fatty acid metabolism and for conferring resistance to psoriasis in mice. Perturbation of signal transducer and activator of transcription 6 (STAT6) diminishes the homeostatic levels of LXR and PPARγ. Furthermore, mice lacking STAT6, interleukin 4 receptor alpha (IL-4Rα), or IL-13, but not IL-4, exhibit increased susceptibility to psoriasis. Under steady state, innate lymphoid cells (ILCs) are the primary producers of IL-13. In human skin, inhibiting tonic type 2 immunity exacerbates psoriasis-like inflammation and IL-17A, while activating LXR or PPARγ inhibits them. Hence, we propose that tonic type 2 immunity, driven by IL-13-producing ILCs, represents a crucial tissue checkpoint that represses autoimmunity and maintains lipid homeostasis in the skin. [Display omitted] •Psoriasis induces a downregulation of fatty acid metabolism and Th2 signature genes•LXR and PPARγ are required for the resistance to psoriasis and lipid homeostasis•IL-13-producing ILCs are responsible for tonic type 2 immunity in normal skin•Inhibiting tonic type 2 immunity worsens psoriatic inflammation in mice and humans Lee et al. show that fatty acid dysregulation occurs in psoriatic skin. Lack of LXR or PPARγ exacerbates psoriasis progression, and LXR and PPARγ homeostasis is maintained by tonic type 2 immunity. IL-13-producing ILCs are in charge of tonic type 2 immunity and contribute to the resistance to autoimmunity. Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid metabolism, as well as Th2 signature. Homeostatic expression of liver X receptor (LXR) and peroxisome proliferator-activated receptor gamma (PPARγ) is essential for maintaining fatty acid metabolism and for conferring resistance to psoriasis in mice. Perturbation of signal transducer and activator of transcription 6 (STAT6) diminishes the homeostatic levels of LXR and PPARγ. Furthermore, mice lacking STAT6, interleukin 4 receptor alpha (IL-4Rα), or IL-13, but not IL-4, exhibit increased susceptibility to psoriasis. Under steady state, innate lymphoid cells (ILCs) are the primary producers of IL-13. In human skin, inhibiting tonic type 2 immunity exacerbates psoriasis-like inflammation and IL-17A, while activating LXR or PPARγ inhibits them. Hence, we propose that tonic type 2 immunity, driven by IL-13-producing ILCs, represents a crucial tissue checkpoint that represses autoimmunity and maintains lipid homeostasis in the skin.Immunoregulatory mechanisms established in the lymphoid organs are vital for preventing autoimmunity. However, the presence of similar mechanisms in non-lymphoid tissues remains unclear. Through transcriptomic and lipidomic analyses, we find a negative association between psoriasis and fatty acid metabolism, as well as Th2 signature. Homeostatic expression of liver X receptor (LXR) and peroxisome proliferator-activated receptor gamma (PPARγ) is essential for maintaining fatty acid metabolism and for conferring resistance to psoriasis in mice. Perturbation of signal transducer and activator of transcription 6 (STAT6) diminishes the homeostatic levels of LXR and PPARγ. Furthermore, mice lacking STAT6, interleukin 4 receptor alpha (IL-4Rα), or IL-13, but not IL-4, exhibit increased susceptibility to psoriasis. Under steady state, innate lymphoid cells (ILCs) are the primary producers of IL-13. In human skin, inhibiting tonic type 2 immunity exacerbates psoriasis-like inflammation and IL-17A, while activating LXR or PPARγ inhibits them. Hence, we propose that tonic type 2 immunity, driven by IL-13-producing ILCs, represents a crucial tissue checkpoint that represses autoimmunity and maintains lipid homeostasis in the skin. |
ArticleNumber | 114364 |
Author | Bok, Jahyun Kim, Tae-Gyun Lee, Haeseung Kim, Sung-Hee Park, Miso Kim, Jiyeon Chung, Yeonseok Lee, Myunggyo Yeo, Hyeonuk Kim, Daehong Kim, Min-Ju Kwon, Sung Won Ronchese, Franca Kim, Mina Kim, Hye Young Lee, Jeong-Eun Lamiable, Olivier Ochiai, Sotaro |
Author_xml | – sequence: 1 givenname: Jeong-Eun surname: Lee fullname: Lee, Jeong-Eun organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 2 givenname: Mina surname: Kim fullname: Kim, Mina organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 3 givenname: Sotaro surname: Ochiai fullname: Ochiai, Sotaro organization: Malaghan Institute of Medical Research, Wellington, New Zealand – sequence: 4 givenname: Sung-Hee surname: Kim fullname: Kim, Sung-Hee organization: Department of Dermatology, Cutaneous Biology Research Institute, Yonsei University College of Medicine, Seoul, Republic of Korea – sequence: 5 givenname: Hyeonuk surname: Yeo fullname: Yeo, Hyeonuk organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 6 givenname: Jahyun surname: Bok fullname: Bok, Jahyun organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 7 givenname: Jiyeon surname: Kim fullname: Kim, Jiyeon organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 8 givenname: Miso surname: Park fullname: Park, Miso organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 9 givenname: Daehong surname: Kim fullname: Kim, Daehong organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 10 givenname: Olivier surname: Lamiable fullname: Lamiable, Olivier organization: Malaghan Institute of Medical Research, Wellington, New Zealand – sequence: 11 givenname: Myunggyo surname: Lee fullname: Lee, Myunggyo organization: College of Pharmacy and Research Institute for Drug Development, Pusan National University, Busan, Republic of Korea – sequence: 12 givenname: Min-Ju surname: Kim fullname: Kim, Min-Ju organization: College of Pharmacy and Research Institute for Drug Development, Pusan National University, Busan, Republic of Korea – sequence: 13 givenname: Hye Young surname: Kim fullname: Kim, Hye Young organization: College of Medicine, Seoul National University, Seoul, Republic of Korea – sequence: 14 givenname: Franca surname: Ronchese fullname: Ronchese, Franca email: fronchese@malaghan.org.nz organization: Malaghan Institute of Medical Research, Wellington, New Zealand – sequence: 15 givenname: Sung Won surname: Kwon fullname: Kwon, Sung Won email: swkwon@snu.ac.kr organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea – sequence: 16 givenname: Haeseung surname: Lee fullname: Lee, Haeseung email: haeseung@pusan.ac.kr organization: College of Pharmacy and Research Institute for Drug Development, Pusan National University, Busan, Republic of Korea – sequence: 17 givenname: Tae-Gyun surname: Kim fullname: Kim, Tae-Gyun email: tgmed83@yuhs.ac organization: Department of Dermatology, Cutaneous Biology Research Institute, Yonsei University College of Medicine, Seoul, Republic of Korea – sequence: 18 givenname: Yeonseok orcidid: 0000-0001-5780-4841 surname: Chung fullname: Chung, Yeonseok email: yeonseok@snu.ac.kr organization: Institute of Pharmaceutical Sciences and College of Pharmacy, Seoul National University, Seoul, Republic of Korea |
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Keywords | CP: Immunology tonic type 2 immunity fatty acid metabolism psoriasis PPARγ LXR |
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Title | Tonic type 2 immunity is a critical tissue checkpoint controlling autoimmunity in the skin |
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