Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

Research Article

Interleukin (IL)-23, IL-31, and IL-33 Play a Role in the Course of Autoimmune Endocrine Diseases

Author(s): Szymon Janyga*, Dariusz Kajdaniuk, Zenon Czuba, Monika Ogrodowczyk-Bobik, Agata Urbanek, Beata Kos-Kudła and Bogdan Marek*

Volume 24, Issue 5, 2024

Published on: 19 September, 2023

Page: [585 - 595] Pages: 11

DOI: 10.2174/1871530323666230908143521

Price: $65

conference banner
Abstract

Background: Interleukins (IL)-23, 31, and 33 are involved in the regulation of T helper 17 (Th17)/regulatory T (Treg) cells balance. The role of IL-23, 31 and 33 in non-endocrine autoimmune diseases has been confirmed. Data on the involvement of these cytokines in endocrine autoimmune diseases are limited.

Objective: This study aimed to determine the involvement of cytokines regulating the T helper 17 (Th17)/regulatory T (Treg) cells axis in the course of autoimmune endocrine diseases.

Methods: A total number of 80 participants were divided into 4 groups: the autoimmune polyendocrine syndrome (APS) group consisting of APS type 2 (APS-2) and type 3 (APS-3) subgroups, the Hashimoto's thyroiditis (HT) group, the Graves’ disease (GD) group and the control (C) group.

Fifteen cytokines related to Th17 and Treg lymphocytes were determined in the serum of all participants. Results: Higher levels of IL-23 and IL-31 were found in the APS, GD, and HT groups compared to the C group. Higher levels of IL-23 and IL-31 were also observed in the APS-2 group, in contrast to the APS-3 group. Correlation analysis of variables in the groups showed a statistically significant correlation between the cytokines IL-23, IL-31, and IL-33 in the APS and APS-2 groups, but no correlation in the APS-3 and C groups.

Conclusion: IL-23 and IL-31 are independent factors in the course of HT, GD, and APS-2, in contrast to APS-3. The positive correlation between IL-23 and IL-31, IL-23 and IL-33, and between IL-31 and IL-33 in the APS, APS-2 groups, but the lack of correlation in the APS-3 and C groups may further suggest the involvement of these cytokines in the course of Addison's disease.

Keywords: IL-23, IL-31, IL-33, autoimmune thyroid disease, autoimmune polyendocrine syndrome, Addison’s disease, Th17 cells, Treg cells.

Graphical Abstract
[1]
Jameson, J.L. Harrison’s endocrinology, 4th ed; McGraw-Hill Education Medica: New York, 2017, pp. 405-412.
[2]
Szeliga, A.; Calik-Ksepka, A.; Maciejewska-Jeske, M.; Grymowicz, M.; Smolarczyk, K.; Kostrzak, A.; Smolarczyk, R.; Rudnicka, E.; Meczekalski, B. Autoimmune diseases in patients with premature ovarian insufficiency-our current state of knowledge. Int. J. Mol. Sci., 2021, 22(5), 2594.
[http://dx.doi.org/10.3390/ijms22052594] [PMID: 33807517]
[3]
Decmann, A.; Tőke, J.; Csöregh, É.; Gáspárdy, G.; Somogyi, A. Type 3 autoimmune polyglandular syndrome with multiple genetic alterations in a young male patient with type 1 diabetes mellitus. Endokrynol. Pol., 2021, 72(3), 286-287.
[http://dx.doi.org/10.5603/EP.a2021.0035] [PMID: 34010447]
[4]
Jadidi-Niaragh, F.; Mirshafiey, A. The deviated balance between regulatory T cell and Th17 in autoimmunity. Immunopharmacol. Immunotoxicol., 2012, 34(5), 727-739.
[http://dx.doi.org/10.3109/08923973.2011.619987] [PMID: 22316060]
[5]
Li, Q.; Wang, B.; Mu, K.; Zhang, J.A. The pathogenesis of thyroid autoimmune diseases: New T lymphocytes – Cytokines circuits beyond the Th1−Th2 paradigm. J. Cell. Physiol., 2019, 234(3), 2204-2216.
[http://dx.doi.org/10.1002/jcp.27180] [PMID: 30246383]
[6]
Janyga, S.; Marek, B.; Kajdaniuk, D.; Ogrodowczyk-Bobik, M.; Urbanek, A.; Bułdak, Ł. CD4+ cells in autoimmune thyroid disease. Endokrynol. Pol., 2021, 72(5), 572-583.
[http://dx.doi.org/10.5603/EP.a2021.0076] [PMID: 34647609]
[7]
Kawashima, A.; Tanigawa, K.; Akama, T.; Yoshihara, A.; Ishii, N.; Suzuki, K. Innate immune activation and thyroid autoimmunity. J. Clin. Endocrinol. Metab., 2011, 96(12), 3661-3671.
[http://dx.doi.org/10.1210/jc.2011-1568] [PMID: 21956420]
[8]
González-Amaro, R.; Marazuela, M. T regulatory (Treg) and T helper 17 (Th17) lymphocytes in thyroid autoimmunity. Endocrine, 2016, 52(1), 30-38.
[http://dx.doi.org/10.1007/s12020-015-0759-7] [PMID: 26475497]
[9]
Luty, J.; Ruckemann-Dziurdzińska, K.; Witkowski, J.M.; Bryl, E. Immunological aspects of autoimmune thyroid disease – Complex interplay between cells and cytokines. Cytokine, 2019, 116, 128-133.
[http://dx.doi.org/10.1016/j.cyto.2019.01.003] [PMID: 30711852]
[10]
Bedoya, S.K.; Lam, B.; Lau, K.; Larkin, J., III Th17 cells in immunity and autoimmunity. Clin. Dev. Immunol., 2013, 2013, 1-16.
[http://dx.doi.org/10.1155/2013/986789] [PMID: 24454481]
[11]
Yasuda, K.; Takeuchi, Y.; Hirota, K. The pathogenicity of Th17 cells in autoimmune diseases. Semin. Immunopathol., 2019, 41(3), 283-297.
[http://dx.doi.org/10.1007/s00281-019-00733-8] [PMID: 30891627]
[12]
Tang, C.; Chen, S.; Qian, H.; Huang, W. Interleukin-23: As a drug target for autoimmune inflammatory diseases. Immunology, 2012, 135(2), 112-124.
[http://dx.doi.org/10.1111/j.1365-2567.2011.03522.x] [PMID: 22044352]
[13]
Kondo, N.; Kuroda, T.; Kobayashi, D. Cytokine networks in the pathogenesis of rheumatoid arthritis. Int. J. Mol. Sci., 2021, 22(20), 10922.
[http://dx.doi.org/10.3390/ijms222010922] [PMID: 34681582]
[14]
Vecellio, M.; Hake, V.X.; Davidson, C.; Carena, M.C.; Wordsworth, B.P.; Selmi, C. The IL-17/IL-23 axis and its genetic contribution to psoriatic arthritis. Front. Immunol., 2021, 11, 596086.
[http://dx.doi.org/10.3389/fimmu.2020.596086] [PMID: 33574815]
[15]
Liu, T.; Li, S.; Ying, S.; Tang, S.; Ding, Y.; Li, Y.; Qiao, J.; Fang, H. The IL-23/IL-17 pathway in inflammatory skin diseases: From bench to bedside. Front. Immunol., 2020, 11, 594735.
[http://dx.doi.org/10.3389/fimmu.2020.594735] [PMID: 33281823]
[16]
Tsukazaki, H.; Kaito, T. The role of the IL-23/IL-17 pathway in the pathogenesis of spondyloarthritis. Int. J. Mol. Sci., 2020, 21(17), 6401.
[http://dx.doi.org/10.3390/ijms21176401] [PMID: 32899140]
[17]
Mandour, M.; Chen, S.; van de Sande, M.G.H. The role of the IL-23/IL-17 axis in disease initiation in spondyloarthritis: lessons learned from animal models. Front. Immunol., 2021, 12, 618581.
[http://dx.doi.org/10.3389/fimmu.2021.618581] [PMID: 34267743]
[18]
Schinocca, C.; Rizzo, C.; Fasano, S.; Grasso, G.; La Barbera, L.; Ciccia, F.; Guggino, G. Role of the IL-23/IL-17 pathway in rheumatic diseases: An overview. Front. Immunol., 2021, 12, 637829.
[http://dx.doi.org/10.3389/fimmu.2021.637829] [PMID: 33692806]
[19]
Murdaca, G.; Greco, M.; Tonacci, A.; Negrini, S.; Borro, M.; Puppo, F.; Gangemi, S. IL-33/IL-31 axis in immune-mediated and allergic diseases. Int. J. Mol. Sci., 2019, 20(23), 5856.
[http://dx.doi.org/10.3390/ijms20235856] [PMID: 31766607]
[20]
Di Salvo, E.; Ventura-Spagnolo, E.; Casciaro, M.; Navarra, M.; Gangemi, S. IL-33/IL-31 axis: A potential inflammatory pathway. Mediators Inflamm., 2018, 2018, 1-8.
[http://dx.doi.org/10.1155/2018/3858032] [PMID: 29713240]
[21]
Gołąb, J.; Jakóbisiak, M.; Firczuk, M. Cytokiny. In: Immunologia, 7th ed; Gołąb, J.; Jakóbisiak, M.; Lasek, W., Eds.; Wydawnictwo Naukowe PWN SA: Warszawa , 2017; pp. 159-198.
[22]
Dubin, C.; Del Duca, E.; Guttman-Yassky, E. The IL-4, IL-13 and IL-31 pathways in atopic dermatitis. Expert Rev. Clin. Immunol., 2021, 17(8), 835-852.
[http://dx.doi.org/10.1080/1744666X.2021.1940962] [PMID: 34106037]
[23]
De Martinis, M.; Sirufo, M.M.; Suppa, M.; Ginaldi, L. IL-33/IL-31 axis in osteoporosis. Int. J. Mol. Sci., 2020, 21(4), 1239.
[http://dx.doi.org/10.3390/ijms21041239] [PMID: 32069819]
[24]
Furue, M.; Yamamura, K.; Kido-Nakahara, M.; Nakahara, T.; Fukui, Y. Emerging role of interleukin-31 and interleukin-31 receptor in pruritus in atopic dermatitis. Allergy, 2018, 73(1), 29-36.
[http://dx.doi.org/10.1111/all.13239] [PMID: 28670717]
[25]
Andoh, A.; Yagi, Y.; Shioya, M.; Nishida, A.; Tsujikawa, T.; Fujiyama, Y. Mucosal cytokine network in inflammatory bowel disease. World J. Gastroenterol., 2008, 14(33), 5154-5161.
[http://dx.doi.org/10.3748/wjg.14.5154] [PMID: 18777592]
[26]
Rabenhorst, A.; Hartmann, K. Interleukin-31: A novel diagnostic marker of allergic diseases. Curr. Allergy Asthma Rep., 2014, 14(4), 423.
[http://dx.doi.org/10.1007/s11882-014-0423-y] [PMID: 24510535]
[27]
Petra, A.I.; Tsilioni, I.; Taracanova, A.; Katsarou-Katsari, A.; Theoharides, T.C. Interleukin 33 and interleukin 4 regulate interleukin 31 gene expression and secretion from human laboratory of allergic diseases 2 mast cells stimulated by substance P and/or immunoglobulin E. Allergy Asthma Proc., 2018, 39(2), 153-160.
[http://dx.doi.org/10.2500/aap.2018.38.4105] [PMID: 29490771]
[28]
Maier, E.; Werner, D.; Duschl, A.; Bohle, B.; Horejs-Hoeck, J. Human Th2 but not Th9 cells release IL-31 in a STAT6/NF-κB-dependent way. J. Immunol., 2014, 193(2), 645-654.
[http://dx.doi.org/10.4049/jimmunol.1301836] [PMID: 24943220]
[29]
Catalan-Dibene, J.; McIntyre, L.L.; Zlotnik, A. Interleukin 30 to interleukin 40. J. Interferon Cytokine Res., 2018, 38(10), 423-439.
[http://dx.doi.org/10.1089/jir.2018.0089] [PMID: 30328794]
[30]
Martin, S.J. Cell death and inflammation: The case for IL-1 family cytokines as the canonical DAMPs of the immune system. FEBS J., 2016, 283(14), 2599-2615.
[http://dx.doi.org/10.1111/febs.13775] [PMID: 27273805]
[31]
Braun, H.; Afonina, I.S.; Mueller, C.; Beyaert, R. Dichotomous function of IL-33 in health and disease: From biology to clinical implications. Biochem. Pharmacol., 2018, 148, 238-252.
[http://dx.doi.org/10.1016/j.bcp.2018.01.010] [PMID: 29309756]
[32]
Hodzic, Z.; Schill, E.M.; Bolock, A.M.; Good, M. IL-33 and the intestine: The good, the bad, and the inflammatory. Cytokine, 2017, 100, 1-10.
[http://dx.doi.org/10.1016/j.cyto.2017.06.017] [PMID: 28687373]
[33]
Schmitz, J.; Owyang, A.; Oldham, E.; Song, Y.; Murphy, E.; McClanahan, T.K.; Zurawski, G.; Moshrefi, M.; Qin, J.; Li, X.; Gorman, D.M.; Bazan, J.F.; Kastelein, R.A. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity, 2005, 23(5), 479-490.
[http://dx.doi.org/10.1016/j.immuni.2005.09.015] [PMID: 16286016]
[34]
Halim, T.Y.F.; Steer, C.A.; Mathä, L.; Gold, M.J.; Martinez-Gonzalez, I.; McNagny, K.M.; McKenzie, A.N.J.; Takei, F. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity, 2014, 40(3), 425-435.
[http://dx.doi.org/10.1016/j.immuni.2014.01.011] [PMID: 24613091]
[35]
Cayrol, C.; Girard, J.P. Interleukin-33 (IL-33): A nuclear cytokine from the IL-1 family. Immunol. Rev., 2018, 281(1), 154-168.
[http://dx.doi.org/10.1111/imr.12619] [PMID: 29247993]
[36]
Manglani, M.; Rua, R.; Hendricksen, A.; Braunschweig, D.; Gao, Q.; Tan, W.; Houser, B.; McGavern, D.B.; Oh, K. Method to quantify cytokines and chemokines in mouse brain tissue using Bio-Plex multiplex immunoassays. Methods, 2019, 158, 22-26.
[http://dx.doi.org/10.1016/j.ymeth.2019.02.007] [PMID: 30742997]
[37]
Stanisz, A. Ed.; Affordable statistics course; StatSoft Polska: Krakow, 2007, Vol. 1, pp. 352-433.
[38]
Moczko, J.; Breborowicz, G. Eds.; Not just biostatistics…; Scientific Publishing House: Poznań, 2010, pp. 98-185.
[39]
Schmuller, J. Ed.; Statistical analysis in Excel; Helion: Gliwice, 2020, pp. 266-330.
[40]
Rabiej, M. Ed.; Statistical analysis with Statistica and Excel; Helion: Gliwice, 2018, pp. 310-380.
[41]
Altman, D.G. Ed.; Practical statistics for medical research; Chapman and Hall: London, 1991, pp. 277-321.
[42]
Fleiss, J.L.; Levin, B.; Paik, M.C. Eds.; Statistical Methods for Rates and Proportions,, 1st ed; Wiley: Hoboken, 2003, pp. 624-760.
[http://dx.doi.org/10.1002/0471445428]
[43]
Campbell, I. Chi-squared and Fisher–Irwin tests of two-by-two tables with small sample recommendations. Stat. Med., 2007, 26(19), 3661-3675.
[http://dx.doi.org/10.1002/sim.2832] [PMID: 17315184]
[44]
Altman, D.G. Ed.; Statistics with confidence: Confidence intervals and statistical guidelines, 2nd ed; BMJ Books: London, 2011, pp. 73-92.
[45]
Malinski, M.; Szymszal, J. Eds.; Modern mathematical statistics in medicine in spreadsheets; Publishing House of the Medical University of Silesia: Katowice, 1999, pp. 278-330.
[46]
Ghoreschi, K.; Laurence, A.; Yang, X.P.; Tato, C.M.; McGeachy, M.J.; Konkel, J.E.; Ramos, H.L.; Wei, L.; Davidson, T.S.; Bouladoux, N.; Grainger, J.R.; Chen, Q.; Kanno, Y.; Watford, W.T.; Sun, H.W.; Eberl, G.; Shevach, E.M.; Belkaid, Y.; Cua, D.J.; Chen, W.; O’Shea, J.J. Generation of pathogenic TH17 cells in the absence of TGF-β signalling. Nature, 2010, 467(7318), 967-971.
[http://dx.doi.org/10.1038/nature09447] [PMID: 20962846]
[47]
Chen, Z.; Wang, Y.; Ding, X.; Zhang, M.; He, M.; Zhao, Y.; Hu, S.; Zhao, F.; Wang, J.; Xie, B.; Shi, B. The proportion of peripheral blood Tregs among the CD4+ T cells of autoimmune thyroid disease patients: A meta-analysis. Endocr. J., 2020, 67(3), 317-326.
[http://dx.doi.org/10.1507/endocrj.EJ19-0307] [PMID: 31827051]
[48]
Rai, V.K.; Sharma, A.; Upadhyay, D.K.; Gupta, G.D.; Narang, R.K. IL-23/Th17 axis: A potential therapeutic target of psoriasis. Curr. Drug Res. Rev., 2022, 14(1), 24-36.
[http://dx.doi.org/10.2174/2589977513666210707114520] [PMID: 34238181]
[49]
Cai, T.; Wang, G.; Yang, Y.; Mu, K.; Zhang, J.; Jiang, Y.; Zhang, J.A. Association between polymorphisms of IL-23/IL-17 pathway and clinical phenotypes of autoimmune thyroid diseases. Iran. J. Immunol., 2022, 19(2), 139-149.
[PMID: 35767887]
[50]
Farhangi, M.; Tajmiri, S. The correlation between inflammatory and metabolic parameters with thyroid function in patients with Hashimoto’s thyroiditis: the potential role of interleukin 23 (IL-23) and vascular endothelial growth factor (VEGF) - 1. Acta Endocrinol., 2018, 14(2), 163-168.
[http://dx.doi.org/10.4183/aeb.2018.163] [PMID: 31149253]
[51]
Zheng, T.; Xu, C.; Mao, C.; Mou, X.; Wu, F.; Wang, X.; Bu, L.; Zhou, Y.; Luo, X.; Lu, Q.; Liu, H.; Yuan, G.; Wang, S.; Chen, D.; Xiao, Y. Increased Interleukin-23 in Hashimoto’s thyroiditis disease induces autophagy suppression and reactive oxygen species accumulation. Front. Immunol., 2018, 9, 96.
[http://dx.doi.org/10.3389/fimmu.2018.00096] [PMID: 29434604]
[52]
Hasan, G.A.; Altamemi, I.A. CTLA-4 polymorphism along with proinflammatory cytokines in autoimmune thyroiditis disease. Wiad. Lek., 2022, 75(3), 577-583.
[http://dx.doi.org/10.36740/WLek202203103] [PMID: 35522861]
[53]
Ruggeri, R.M.; Saitta, S.; Cristani, M.; Giovinazzo, S.; Tigano, V.; Trimarchi, F.; Benvenga, S.; Gangemi, S. Serum interleukin-23 (IL-23) is increased in Hashimoto’s thyroiditis. Endocr. J., 2014, 61(4), 359-363.
[http://dx.doi.org/10.1507/endocrj.EJ13-0484] [PMID: 24476945]
[54]
Zake, T.; Skuja, S.; Kalere, I.; Konrade, I.; Groma, V. Upregulated tissue expression of T helper (Th) 17 pathogenic interleukin (IL)-23 and IL-1β in Hashimoto’s thyroiditis but not in Graves’ disease. Endocr. J., 2019, 66(5), 423-430.
[http://dx.doi.org/10.1507/endocrj.EJ18-0396] [PMID: 30814438]
[55]
Zheng, L.; Ye, P.; Liu, C. The role of the IL-23/IL-17 axis in the pathogenesis of Graves’ disease. Endocr. J., 2013, 60(5), 591-597.
[http://dx.doi.org/10.1507/endocrj.EJ12-0264] [PMID: 23327801]
[56]
de J Guerrero-García. J.; Rojas-Mayorquín, A.E.; Valle, Y.; Padilla-Gutiérrez, J.R.; Castañeda-Moreno, V.A.; Mireles-Ramírez, M.A.; Muñoz-Valle, J.F.; Ortuño-Sahagún, D. Decreased serum levels of sCD40L and IL-31 correlate in treated patients with Relapsing-Remitting Multiple Sclerosis. Immunobiology, 2018, 223(1), 135-141.
[http://dx.doi.org/10.1016/j.imbio.2017.10.001] [PMID: 29050818]
[57]
Pastor, B.I.; de Almeid, F.A.E.; Murillo, W.G.; de Medeiros, J.W.L.G.; Nogueira, B.W.; Schatzmann, P.J.P.; Becker, J.; Nascimento, O.J.M.; Magno, G.M.V. Interleukin-31 and soluble CD40L: New candidate serum biomarkers that predict therapeutic response in multiple sclerosis. Neurol. Sci., 2022, 43(11), 6271-6278.
[http://dx.doi.org/10.1007/s10072-022-06276-5] [PMID: 35849199]
[58]
García-Arellano, S.; Hernández-Palma, L.A.; Cerpa-Cruz, S.; Sánchez-Zuno, G.A.; Herrera-Godina, M.G.; Muñoz-Valle, J.F. The novel role of MIF in the secretion of IL-25, IL-31, and IL-33 from PBMC of patients with rheumatoid arthritis. Molecules, 2021, 26(16), 4968.
[http://dx.doi.org/10.3390/molecules26164968] [PMID: 34443554]
[59]
Liu, X.; Xiao, Y.; Pan, Y.; Li, H.; Zheng, S.G.; Su, W. The role of the IL-33/ST2 axis in autoimmune disorders: Friend or foe? Cytokine Growth Factor Rev., 2019, 50, 60-74.
[http://dx.doi.org/10.1016/j.cytogfr.2019.04.004] [PMID: 31085085]
[60]
Abdelati, A.A.; Deghady, A.A.E.; Abdelhady, A.M.; Bastawy, R.A.; Shaaban, A. Patterns of interstitial lung disease in Egyptian patients with systemic sclerosis: Relation to disease parameters. Curr. Rheumatol. Rev., 2023, 19(2), 189-196.
[http://dx.doi.org/10.2174/1573397118666220818095927] [PMID: 35984025]
[61]
De la Fuente, M.; MacDonald, T.T.; Hermoso, M.A. The IL-33/ST2 axis: Role in health and disease. Cytokine Growth Factor Rev., 2015, 26(6), 615-623.
[http://dx.doi.org/10.1016/j.cytogfr.2015.07.017] [PMID: 26271893]
[62]
Préfontaine, D.; Nadigel, J.; Chouiali, F.; Audusseau, S.; Semlali, A.; Chakir, J.; Martin, J.G.; Hamid, Q. Increased IL-33 expression by epithelial cells in bronchial asthma. J. Allergy Clin. Immunol., 2010, 125(3), 752-754.
[http://dx.doi.org/10.1016/j.jaci.2009.12.935] [PMID: 20153038]
[63]
Celik, H.T.; Abusoglu, S.; Burnik, S.F.; Sezer, S.; Serdar, M.A.; Ercan, M.; Uguz, N.; Avcikucuk, M.; Ceylan, B.; Yildirimkaya, M. Increased serum interleukin-33 levels in patients with Graves’ disease. Endocr. Regul., 2013, 47(2), 57-64.
[http://dx.doi.org/10.4149/endo_2013_02_57] [PMID: 23641786]
[64]
Wang, X.; Shao, X.; Liu, X.; Qin, Q.; Xu, J.; Zhang, J.A. Dysregulated Interleukin -33/ST2 pathway perpetuates chronic inflammation in Hashimoto’s thyroiditis. Endocr. Metab. Immune Disord. Drug Targets, 2019, 19(7), 1012-1021.
[http://dx.doi.org/10.2174/1871530319666190226164309] [PMID: 30819087]
[65]
Rak, G.D.; Osborne, L.C.; Siracusa, M.C.; Kim, B.S.; Wang, K.; Bayat, A.; Artis, D.; Volk, S.W. IL-33-dependent group 2 innate lymphoid cells promote cutaneous wound healing. J. Invest. Dermatol., 2016, 136(2), 487-496.
[http://dx.doi.org/10.1038/JID.2015.406] [PMID: 26802241]
[66]
Pascual-Reguant, A.; Bayat Sarmadi, J.; Baumann, C.; Noster, R.; Cirera-Salinas, D.; Curato, C.; Pelczar, P.; Huber, S.; Zielinski, C.E.; Löhning, M.; Hauser, A.E.; Esplugues, E. TH17 cells express ST2 and are controlled by the alarmin IL-33 in the small intestine. Mucosal Immunol., 2017, 10(6), 1431-1442.
[http://dx.doi.org/10.1038/mi.2017.5] [PMID: 28198366]
[67]
Schiering, C.; Krausgruber, T.; Chomka, A.; Fröhlich, A.; Adelmann, K.; Wohlfert, E.A.; Pott, J.; Griseri, T.; Bollrath, J.; Hegazy, A.N.; Harrison, O.J.; Owens, B.M.J.; Löhning, M.; Belkaid, Y.; Fallon, P.G.; Powrie, F. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature, 2014, 513(7519), 564-568.
[http://dx.doi.org/10.1038/nature13577] [PMID: 25043027]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy