دورية أكاديمية
Meteorin-like protein/METRNL/Interleukin-41 ameliorates atopic dermatitis-like inflammation.
العنوان: | Meteorin-like protein/METRNL/Interleukin-41 ameliorates atopic dermatitis-like inflammation. |
---|---|
المؤلفون: | Huang D; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China., Liu X; Department of Dermatology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, Guangzhou, Guangdong, China., Gao X; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China.; Center of Clinical Laboratory Medicine, Zhongda Hospital, Southeast University, Nanjing, China., Choi CK; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China., Giglio G; Bridge Institute of Experimental Tumor Therapy, West German Cancer Center, University Hospital Essen, Essen, Germany.; Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany., Farah L; Bridge Institute of Experimental Tumor Therapy, West German Cancer Center, University Hospital Essen, Essen, Germany.; Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany., Leung TF; Department of Paediatrics, The Chinese University of Hong Kong, Hong Kong, China., Wong KC; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China., Kan LL; Institute of Chinese Medicine and State Key Laboratory of Research on Bioactivities and Clinical Applications of Medicinal Plants, The Chinese University of Hong Kong, Hong Kong, China., Chong JW; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China., Meng QJ; Welcome Centre for Cell Matrix Research, Division of Cell Matrix Biology and Regenerative Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK.; Centre for Biological Timing, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, UK., Liao J; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China., Cheung PF; Bridge Institute of Experimental Tumor Therapy, West German Cancer Center, University Hospital Essen, Essen, Germany.; Division of Solid Tumor Translational Oncology, German Cancer Consortium (DKTK, partner site Essen) and German Cancer Research Center, DKFZ, Heidelberg, Germany.; Spatiotemporal tumor heterogeneity, German Cancer Consortium (DKTK), A Partnership Between German Cancer Research Center (DKFZ) and University Hospital, Essen, Germany., Wong CK; Department of Chemical Pathology, The Chinese University of Hong Kong, Hong Kong, China.; Institute of Chinese Medicine and State Key Laboratory of Research on Bioactivities and Clinical Applications of Medicinal Plants, The Chinese University of Hong Kong, Hong Kong, China. |
المصدر: | Allergy [Allergy] 2024 May 10. Date of Electronic Publication: 2024 May 10. |
Publication Model: | Ahead of Print |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: Wiley-Blackwell Country of Publication: Denmark NLM ID: 7804028 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1398-9995 (Electronic) Linking ISSN: 01054538 NLM ISO Abbreviation: Allergy Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Copenhagen : Wiley-Blackwell Original Publication: Copenhagen, Munksgaard. |
مستخلص: | Background: Meteorin-like protein (METRNL)/Interleukin-41 (IL-41) is a novel immune-secreted cytokine/myokine involved in several inflammatory diseases. However, how METRNL exerts its regulatory properties on skin inflammation remains elusive. This study aims to elucidate the functionality and regulatory mechanism of METRNL in atopic dermatitis (AD). Methods: METRNL levels were determined in skin and serum samples from patients with AD and subsequently verified in the vitamin D3 analogue MC903-induced AD-like mice model. The cellular target of METRNL activity was identified by multiplex immunostaining, single-cell RNA-seq and RNA-seq. Results: METRNL was significantly upregulated in lesions and serum of patients with dermatitis compared to healthy controls (p <.05). Following repeated MC903 exposure, AD model mice displayed elevated levels of METRNL in both ears and serum. Administration of recombinant murine METRNL protein (rmMETRNL) ameliorated allergic skin inflammation and hallmarks of AD in mice, whereas blocking of METRNL signaling led to the opposite. METRNL enhanced β-Catenin activation, limited the expression of Th2-related molecules that attract the accumulation of Arginase-1 (Arg1) hi macrophages, dendritic cells, and activated mast cells. Conclusions: METRNL can bind to KIT receptor and subsequently alleviate the allergic inflammation of AD by inhibiting the expansion of immune cells, and downregulating inflammatory gene expression by regulating the level of active WNT pathway molecule β-Catenin. (© 2024 The Authors. Allergy published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.) |
References: | Esaki H, Brunner PM, Renert‐Yuval Y, et al. Early‐onset pediatric atopic dermatitis is TH2 but also TH17 polarized in skin. J Allergy Clin Immunol. 2016;138:1639‐1651. Vandeghinste N, Klattig J, Jagerschmidt C, et al. Neutralization of IL‐17C reduces skin inflammation in mouse models of psoriasis and atopic dermatitis. J Invest Dermatol. 2018;138:1555‐1563. Ushach I, Burkhardt AM, Martinez C, et al. METEORIN‐LIKE is a cytokine associated with barrier tissues and alternatively activated macrophages. Clin Immunol Orlando Fla. 2015;156:119‐127. Baht GS, Bareja A, Lee DE, et al. Meteorin‐like facilitates skeletal muscle repair through a Stat3/IGF‐1 mechanism. Nat Metab. 2020;2:278‐289. Lee DE, McKay LK, Bareja A, et al. Meteorin‐like is an injectable peptide that can enhance regeneration in aged muscle through immune‐driven fibro/adipogenic progenitor signaling. Nat Commun. 2022;13:7613. Jung TW, Pyun DH, Kim TJ, et al. Meteorin‐like protein (METRNL)/IL‐41 improves LPS‐induced inflammatory responses via AMPK or PPARδ–mediated signaling pathways. Adv Med Sci. 2021;66:155‐161. Zheng S, Li Z, Song J, et al. Endothelial METRNL determines circulating METRNL level and maintains endothelial function against atherosclerosis. Acta Pharm Sin B. 2023;13:1568‐1587. Hu J, He A, Yue X, Zhou M, Zhou Y. METRNL reduced inflammation in sepsis‐induced renal injury via PPARδ‐dependent pathways. Food Sci Technol. 2022;42:e61821. Alizadeh H. Meteorin‐like protein (Metrnl): a metabolic syndrome biomarker and an exercise mediator. Cytokine. 2022;157:155952. Rao RR, Long JZ, White JP, et al. Meteorin‐like is a hormone that regulates immune‐adipose interactions to increase beige fat thermogenesis. Cell. 2014;157:1279‐1291. Guo M, Zhang J, Ma Y, et al. AAV‐mediated nuclear localized PGC1α4 delivery in muscle ameliorates sarcopenia and aging‐associated metabolic dysfunctions. Aging Cell. 2023;22:e13961. Reboll MR, Klede S, Taft MH, et al. Meteorin‐like promotes heart repair through endothelial KIT receptor tyrosine kinase. Science. 2022;376:1343‐1347. Ushach I, Arrevillaga‐Boni G, Heller GN, et al. Meteorin‐like/Meteorin‐Beta is a novel immunoregulatory cytokine associated with inflammation. J Immunol Baltim Md. 1950;2018(201):3669‐3676. Gao X, Leung T‐F, Wong GW‐K, et al. Meteorin‐β/Meteorin like/IL‐41 attenuates airway inflammation in house dust mite‐induced allergic asthma. Cell Mol Immunol. 2022;19:245‐259. Gao X, Chan PK‐S, Wong KC‐Y, et al. Characterization of METRNβ as a novel biomarker of coronavirus disease 2019 severity and prognosis. Front Immunol. 2023;14:1111920. Chen X, Chen X, Yang Y, et al. Protective role of the novel cytokine Metrnl/ interleukin‐41 in host immunity defense during sepsis by promoting macrophage recruitment and modulating Treg/Th17 immune cell balance. Clin Immunol. 2023;254:109690. Knipper JA, Ivens A, Taylor MD. Helminth‐induced Th2 cell dysfunction is distinct from exhaustion and is maintained in the absence of antigen. PLoS Negl Trop Dis. 2019;13:e0007908. Liu Y, Wang H, Taylor M, et al. Classification of human chronic inflammatory skin disease based on single‐cell immune profiling. Sci Immunol. 2022;7:eabl9165. Del Duca E, He H, Liu Y, et al. Intrapatient comparison of atopic dermatitis skin transcriptome shows differences between tape‐strips and biopsies. Allergy. 2024;79:80‐92. Marschall P, Wei R, Segaud J, et al. Dual function of Langerhans cells in skin TSLP‐promoted TFH differentiation in mouse atopic dermatitis. J Allergy Clin Immunol. 2021;147:1778‐1794. Hou T, Sun X, Zhu J, et al. IL‐37 ameliorating allergic inflammation in atopic dermatitis through regulating microbiota and AMPK‐mTOR signaling pathway‐modulated autophagy mechanism. Front Immunol. 2020;11:752. Xu Z, Wang W, Yang T, et al. STOmicsDB: a comprehensive database for spatial transcriptomics data sharing, analysis and visualization. Nucleic Acids Res. 2024;52:D1053‐D1061. Mitamura Y, Reiger M, Kim J, et al. Spatial transcriptomics combined with single‐cell RNA‐sequencing unravels the complex inflammatory cell network in atopic dermatitis. Allergy. 2023;78:2215‐2231. Li M, Hener P, Zhang Z, Kato S, Metzger D, Chambon P. Topical vitamin D3 and low‐calcemic analogs induce thymic stromal lymphopoietin in mouse keratinocytes and trigger an atopic dermatitis. Proc Natl Acad Sci USA. 2006;103:11736‐11741. Brudvik KW, Taskén K. Modulation of T cell immune functions by the prostaglandin E 2 – cAMP pathway in chronic inflammatory states. Br J Pharmacol. 2012;166:411‐419. Chinn AM, Insel PA. Cyclic AMP in dendritic cells: a novel potential target for disease‐modifying agents in asthma and other allergic disorders. Br J Pharmacol. 2020;177:3363‐3377. Baysoy A, Seddu K, Salloum T, et al. The interweaved signatures of common‐gamma‐chain cytokines across immunologic lineages. J Exp Med. 2023;220:e20222052. Luo X, Chen J, Yang H, et al. Dendritic cell immunoreceptor drives atopic dermatitis by modulating oxidized CaMKII‐involved mast cell activation. JCI Insight. 2022;7:e152559. Rinaldi AO, Li M, Barletta E, et al. Household laundry detergents disrupt barrier integrity and induce inflammation in mouse and human skin. Allergy. 2024;79:128‐141. Swindell WR, Sarkar MK, Liang Y, Xing X, Gudjonsson JE. Cross‐disease Transcriptomics: unique IL‐17A signaling in psoriasis lesions and an autoimmune PBMC signature. J Invest Dermatol. 2016;136:1820‐1830. Hashimoto T, Yokozeki H, Karasuyama H, Satoh T. IL‐31‐generating network in atopic dermatitis comprising macrophages, basophils, thymic stromal lymphopoietin, and periostin. J Allergy Clin Immunol. 2023;151:737‐746. Tran LS, Bergot A‐S, Mattarollo SR, Mittal D, Frazer IH. Human papillomavirus E7 Oncoprotein transgenic skin develops an enhanced inflammatory response to 2,4‐dinitrochlorobenzene by an Arginase‐1‐dependent mechanism. J Invest Dermatol. 2014;134:2438‐2446. Kumamoto Y, Camporez JPG, Jurczak MJ, et al. CD301b+ mononuclear phagocytes maintain positive energy balance through secretion of Resistin‐like molecule alpha. Immunity. 2016;45:583‐596. Dichtl S, Lindenthal L, Zeitler L, et al. Lactate and IL6 define separable paths of inflammatory metabolic adaptation. Sci Adv. 2021;7:eabg3505. Vu R, Jin S, Sun P, et al. Wound healing in aged skin exhibits systems‐level alterations in cellular composition and cell‐cell communication. Cell Rep. 2022;40:111155. Rider P, Carmi Y, Guttman O, et al. IL‐1α and IL‐1β recruit different myeloid cells and promote different stages of sterile inflammation. J Immunol. 2011;187:4835‐4843. Gaudet P, Livstone MS, Lewis SE, Thomas PD. Phylogenetic‐based propagation of functional annotations within the gene ontology consortium. Brief Bioinform. 2011;12:449‐462. Nakagomi D, Suzuki K, Meguro K, et al. Matrix metalloproteinase 12 is produced by M2 macrophages and plays important roles in the development of contact hypersensitivity. J Allergy Clin Immunol. 2015;135:1397‐1400. Lennartsson J, Blume‐Jensen P, Hermanson M, Pontén E, Carlberg M, Rönnstrand L. Phosphorylation of Shc by Src family kinases is necessary for stem cell factor receptor/c‐kit mediated activation of the Ras/MAP kinase pathway and c‐fos induction. Oncogene. 1999;18:5546‐5553. Sheikh E, Tran T, Vranic S, Levy A, Bonfil RD. Role and significance of c‐KIT receptor tyrosine kinase in cancer: a review. Biomol Biomed. 2022;22:683‐698. Zeng S, Xu Z, Lipkowitz S, Longley JB. Regulation of stem cell factor receptor signaling by Cbl family proteins (Cbl‐b/c‐Cbl). Blood. 2005;105:226‐232. Keith YH, Honda T, Ono S, et al. Infiltration and local differentiation of bone marrow–derived integrinβ7‐positive mast cell progenitors in atopic dermatitis–like skin. J Allergy Clin Immunol. 2023;151:159‐171.e8. Krishnamoorthy N, Oriss TB, Paglia M, et al. Activation of c‐kit in dendritic cells regulates T helper cell differentiation and allergic asthma. Nat Med. 2008;14:565‐573. Rawat K, Tewari A, Li X, et al. CCL5‐producing migratory dendritic cells guide CCR5+ monocytes into the draining lymph nodes. J Exp Med. 2023;220:e20222129. Speir ML, Bhaduri A, Markov NS, et al. UCSC Cell Browser: visualize your single‐cell data. Bioinformatics. 2021;37:4578‐4580. Manzar N, Khan UK, Goel A, et al. An integrative proteomics approach identifies tyrosine kinase KIT as a therapeutic target for SPINK1‐positive prostate cancer. iScience. 2024;27:108794. Cohen SB, Smith NL, McDougal C, et al. β‐Catenin signaling drives differentiation and Proinflammatory function of IRF8‐dependent dendritic cells. J Immunol. 2015;194:210‐222. Spranger S, Dai D, Horton B, Gajewski TF. Tumor‐residing Batf3 dendritic cells are required for effector T cell trafficking and adoptive T cell therapy. Cancer Cell. 2017;31:711‐723.e4. Lorentz A, Wilke M, Sellge G, et al. IL‐4‐induced priming of human intestinal mast cells for enhanced survival and Th2 cytokine generation is reversible and associated with increased activity of ERK1/2 and c‐Fos1. J Immunol. 2005;174:6751‐6756. Vincent L, Vang D, Nguyen J, et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood. 2013;122:1853‐1862. Mazzoni A, Siraganian RP, Leifer CA, Segal DM. Dendritic cell modulation by mast cells controls the Th1/Th2 balance in responding T Cells1. J Immunol. 2006;177:3577‐3581. Gaudenzio N, Espagnolle N, Mars LT, Liblau R, Valitutti S, Espinosa E. Cell‐cell cooperation at the T helper cell/mast cell immunological synapse. Blood. 2009;114:4979‐4988. Kikuchi‐Ueda T, Kamoshida G, Ubagai T, et al. The TNF‐α of mast cells induces pro‐inflammatory responses during infection with Acinetobacter baumannii. Immunobiology. 2017;222:1025‐1034. Yuan Q, Austen KF, Friend DS, Heidtman M, Boyce JA. Human peripheral blood eosinophils express a functional c‐kit receptor for stem cell factor that stimulates very late antigen 4 (VLA‐4)–mediated cell adhesion to fibronectin and vascular cell adhesion molecule 1 (VCAM‐1). J Exp Med. 1997;186:313‐323. Oliveira SHP, Taub DD, Nagel J, et al. Stem cell factor induces eosinophil activation and degranulation: mediator release and gene array analysis. Blood. 2002;100:4291‐4297. Du Y‐N, Teng J‐M, Zhou T‐H, Du B‐Y, Cai W. Meteorin‐like protein overexpression ameliorates fulminant hepatitis in mice by inhibiting chemokine‐dependent immune cell infiltration. Acta Pharmacol Sin. 2023;44:1404‐1415. Broudy VC, Kovach NL, Bennett LG, Lin N, Jacobsen FW, Kidd PG. Human umbilical vein endothelial cells display high‐affinity c‐kit receptors and produce a soluble form of the c‐kit receptor. Blood. 1994;83:2145‐2152. Fu Z, Dean JW, Xiong L, et al. Mitochondrial transcription factor a in RORγt+ lymphocytes regulate small intestine homeostasis and metabolism. Nat Commun. 2021;12:4462. Kim KL, Seo S, Kim JT, et al. SCF (stem cell factor) and cKIT modulate pathological ocular neovascularization. Arterioscler Thromb Vasc Biol. 2019;39:2120‐2131. Cheng X, Yan J, Liu Y, Wang J, Taubert S. eVITTA: a web‐based visualization and inference toolbox for transcriptome analysis. Nucleic Acids Res. 2021;49:W207‐W215. |
معلومات مُعتمدة: | Jiangsu Province Basic Research Special Fund (Natural Science Foundation), Jiangsu Provincial Department of Science and Technology, China; Innovation and Technology Commission; National Natural Science Foundation of China; Chinese University of Hong Kong |
فهرسة مساهمة: | Keywords: Meteorin‐like protein (METRNL); WNT signaling pathways; atopic dermatitis; cytokines; skin inflammation |
تواريخ الأحداث: | Date Created: 20240510 Latest Revision: 20240510 |
رمز التحديث: | 20240510 |
DOI: | 10.1111/all.16150 |
PMID: | 38727640 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1398-9995 |
---|---|
DOI: | 10.1111/all.16150 |