Generic placeholder image

Endocrine, Metabolic & Immune Disorders - Drug Targets

Editor-in-Chief

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

Research Article

Yiqi Jiedu Xiaoying Decoction Improves Experimental Autoimmune Thyroiditis in Rats by Regulating Th17/Treg Cell Balance

Author(s): Hui Zhu, Shumin Mu*, Shiyin Liu, Yang Cui, Jianyu Ren, Enquan Yang, Lining Wang, Xiaoke Cui and Ailing Ren

Volume 24, Issue 10, 2024

Published on: 04 January, 2024

Page: [1186 - 1196] Pages: 11

DOI: 10.2174/0118715303256311231122094516

Price: $65

conference banner
Abstract

Background: Experimental autoimmune thyroiditis (EAT) is a widely used animal model to study the pathogenesis and treatment of autoimmune thyroid diseases. Yiqi Jiedu Xiaoying Decoction (YJXD) is a traditional Chinese medicine formula with potential immunomodulatory effects. In this study, we investigated the therapeutic effects of YJXD on EAT in rats and explored its underlying mechanisms.

Methods: Female Wistar rats were induced to develop EAT by immunization with thyroglobulin (Tg) and taken sodium iodide water (0.05%) and then treated with YJXD or sodium selenite. HE staining was used to observe the pathological changes of thyroid tissue in EAT rats. Th17 and Treg cell frequencies were analyzed by flow cytometry, and the expression levels of Th17- and Treg-related cytokines and thyroid autoantibody were determined by enzyme-linked immunosorbent assay (ELISA). The expression of Th17- and Treg-related transcriptional factors was detected by real-time polymerase chain reaction (RT-PCR) and Immunohistochemistry (IHC).

Results: Our results demonstrated that treatment with YJXD significantly attenuated the severity of EAT, as evidenced by reduced thyroid gland inflammatory infiltration and decreased serum thyroglobulin autoantibody levels. Importantly, YJXD treatment effectively modulated the Th17/Treg cell balance by suppressing Th17 cell differentiation and promoting Treg cell expansion. Moreover, YJXD was also found to regulate the expression levels of Th17- and Treg-related cytokines and transcriptional factors, further supporting its immunomodulatory effects in EAT.

Conclusion: YJXD exerted therapeutic effects on EAT by regulating the Th17/Treg cell balance, modulating the production of Th17- and Treg-related cytokines and the expression of transcriptional factors.

Keywords: Yiqi Jiedu Xiaoying Decoction, experimental autoimmune thyroiditis (EAT), autoimmune thyroiditis (AIT), cytokines, immunomodulatory effects, transcriptional factor.

Graphical Abstract
[1]
Ragusa, F.; Fallahi, P.; Elia, G.; Gonnella, D.; Paparo, S.R.; Giusti, C.; Churilov, L.P.; Ferrari, S.M.; Antonelli, A. Hashimotos’ thyroiditis: Epidemiology, pathogenesis, clinic and therapy. Best Pract. Res. Clin. Endocrinol. Metab., 2019, 33(6), 101367.
[http://dx.doi.org/10.1016/j.beem.2019.101367] [PMID: 31812326]
[2]
Keefe, G.; Culbreath, K.; Cherella, C.E.; Smith, J.R.; Zendejas, B.; Shamberger, R.C.; Richman, D.M.; Hollowell, M.L.; Modi, B.P.; Wassner, A.J. Autoimmune thyroiditis and risk of malignancy in children with thyroid nodules. Thyroid, 2022, 32(9), 1109-1117.
[http://dx.doi.org/10.1089/thy.2022.0241]
[3]
Al-Mansour, M.; Maglan, A.F.; Altayeb, M.K.; Faraj, L.A.; Felimban, E.A.; Aga, S.S.; Khan, M.A. The risk of developing lymphoma among autoimmune thyroid disorder patients: A cross-section study. Dis. Markers, 2022, 2022, 1-8.
[http://dx.doi.org/10.1155/2022/4354595] [PMID: 35692889]
[4]
Wei, Y.; Fan, Y.; Ga, Y.; Zhang, Y.; Han, J.; Hao, Z. Shaoyao decoction attenuates DSS-induced ulcerative colitis, macrophage and NLRP3 inflammasome activation through the MKP1/NF-kB pathway. Phytomedicine, 2021, 92, 153743.
[http://dx.doi.org/10.1016/j.phymed.2021.153743] [PMID: 34583225]
[5]
Zhao, Y.; Luan, H.; Jiang, H.; Xu, Y.; Wu, X.; Zhang, Y.; Li, R. Gegen Qinlian decoction relieved DSS-induced ulcerative colitis in mice by modulating Th17/Treg cell homeostasis via suppressing IL-6/JAK2/STAT3 signaling. Phytomedicine, 2021, 84, 153519.
[http://dx.doi.org/10.1016/j.phymed.2021.153519] [PMID: 33640781]
[6]
Xie, T.; Liu, X.; Liu, H.; Han, X.; Zhao, J.; Zhou, D.; Wang, Y.; Zhang, H.; Wang, P.; Li, P. LangChuangHeJi decoction ameliorates lupus via preventing accumulation of CD138+ T cells in MRL/lpr mice. Am. J. Transl. Res., 2021, 13(11), 12440-12460.
[PMID: 34956465]
[7]
Sun, J.; Shao, T.J.; Zhang, D.Y.; Huang, X.Q.; Xie, Z.J.; Wen, C.P. Effect of lang-chuang-ding decoction on DNA methylation of CD70 gene promoter in peripheral blood mononuclear cells of female patients with systemic lupus erythematosus. Chin. J. Integr. Med., 2018, 24(5), 348-352.
[http://dx.doi.org/10.1007/s11655-017-2804-2] [PMID: 28497391]
[8]
Li, M.; Li, M.; Lei, J.; Wu, Y.; Li, Z.; Chen, L.; Zhou, C.; Su, J.; Huang, G.; Huang, X.; Zheng, X. Huangqin decoction ameliorates DSS-induced ulcerative colitis: Role of gut microbiota and amino acid metabolism, mTOR pathway and intestinal epithelial barrier. Phytomedicine, 2022, 100, 154052.
[http://dx.doi.org/10.1016/j.phymed.2022.154052] [PMID: 35344714]
[9]
Ma, B.; Chen, D.; Liu, Y.; Zhao, Z.; Wang, J.; Zhou, G.; Xu, K.; Zhu, T.; Wang, Q.; Ma, C. Yanghe decoction suppresses the experimental autoimmune thyroiditis in rats by improving nlrp3 inflammasome and immune dysregulation. Front. Pharmacol., 2021, 12, 645354.
[http://dx.doi.org/10.3389/fphar.2021.645354] [PMID: 34234669]
[10]
Zhou, Y.; Shen, H.; Lan, W.; Shi, Y.; Yao, Q.; Wen, W. Mechanism of Xiaoying Daotan decoction in treating Hashimoto’s thyroiditis based on the Notch/Treg/Th17 pathway. Ann. Transl. Med., 2021, 9(24), 1760.
[http://dx.doi.org/10.21037/atm-21-6253] [PMID: 35071454]
[11]
Sun, H.; Ye, Z.; Li, N.; Jin, F.; Yan, J.; Wu, K. Effect of emodin on T cell subsets in NOD mice with NaI induced experimental autoimmune thyroiditis. Mol. Med. Rep., 2018, 18(5), 4303-4312.
[http://dx.doi.org/10.3892/mmr.2018.9434] [PMID: 30221664]
[12]
Yang, X.; Liu, Z.; Song, N.; Li, M.; Wang, Z.; Cao, H.; Gao, T. Based on mRNA sequencing techniques to explore the molecular mechanism of buzhong yiqi decoction for autoimmune thyroiditis. Comb. Chem. High Throughput Screen., 2024, 27(3), 408-419.
[http://dx.doi.org/10.2174/1386207326666230417120421] [PMID: 37070455]
[13]
Wang, L.; Mu, S. Clinical effect of Fuzheng Jiedu Xiaoying decoctionin treating Hashimoto’s thyroiditis. Shaanxi Journal of Traditional Medicine., 2023, 44(02), 205-208.
[14]
Qin, Y.; Gao, C.; Luo, J. Metabolism characteristics of Th17 and regulatory T cells in autoimmune diseases. Front. Immunol., 2022, 13, 828191.
[http://dx.doi.org/10.3389/fimmu.2022.828191] [PMID: 35281063]
[15]
Yuliasih, Y.; Rahmawati, L.D.; Putri, R.M. Th17/Treg ratio and disease activity in systemic lupus erythematosus. Caspian J. Intern. Med., 2019, 10(1), 65-72.
[http://dx.doi.org/10.22088/cjim.10.1.65] [PMID: 30858943]
[16]
Bhardwaj, S.; Rani, S.; Kumaran, M.S.; Bhatia, A.; Parsad, D. Expression of Th17- and Treg-specific transcription factors in vitiligo patients. Int. J. Dermatol., 2020, 59(4), 474-481.
[http://dx.doi.org/10.1111/ijd.14766] [PMID: 31909498]
[17]
Zhao, L.; Zhou, X.; Zhou, X.; Wang, H.; Gu, L.; Ke, Y.; Zhang, M.; Ji, X.; Yang, X. Low expressions of PD-L1 and CTLA-4 by induced CD4+CD25+ Foxp3+ Tregs in patients with SLE and their correlation with the disease activity. Cytokine, 2020, 133, 155119.
[http://dx.doi.org/10.1016/j.cyto.2020.155119] [PMID: 32535334]
[18]
Jiang, Q.; Yang, G.; Liu, Q.; Wang, S.; Cui, D. Function and role of regulatory T cells in rheumatoid arthritis. Front. Immunol., 2021, 12, 626193.
[http://dx.doi.org/10.3389/fimmu.2021.626193] [PMID: 33868244]
[19]
Goswami, T.K.; Singh, M.; Dhawan, M.; Mitra, S.; Emran, T.B.; Rabaan, A.A.; Mutair, A.A.; Alawi, Z.A.; Alhumaid, S.; Dhama, K. Regulatory T cells (Tregs) and their therapeutic potential against autoimmune disorders – Advances and challenges. Hum. Vaccin. Immunother., 2022, 18(1), 2035117.
[http://dx.doi.org/10.1080/21645515.2022.2035117] [PMID: 35240914]
[20]
Wang, G.; Su, Z.; Li, H.; Xiao, L.; Li, C.; Lian, G. The role of metabolism in Th17 cell differentiation and autoimmune diseases. Int. Immunopharmacol., 2022, 103, 108450.
[http://dx.doi.org/10.1016/j.intimp.2021.108450] [PMID: 34954561]
[21]
Kamali, A.N.; Noorbakhsh, S.M.; Hamedifar, H.; Jadidi-Niaragh, F.; Yazdani, R.; Bautista, J.M.; Azizi, G. A role for Th1-like Th17 cells in the pathogenesis of inflammatory and autoimmune disorders. Mol. Immunol., 2019, 105, 107-115.
[http://dx.doi.org/10.1016/j.molimm.2018.11.015] [PMID: 30502718]
[22]
Guo, K.; Zhang, X. Cytokines that modulate the differentiation of Th17 cells in autoimmune uveitis. J. Immunol. Res., 2021, 2021, 1-19.
[http://dx.doi.org/10.1155/2021/6693542] [PMID: 33816637]
[23]
Lee, G. The balance of Th17 versus Treg cells in autoimmunity. Int. J. Mol. Sci., 2018, 19(3), 730.
[http://dx.doi.org/10.3390/ijms19030730] [PMID: 29510522]
[24]
Vasiliu, I.; Ciobanu-Apostol, D.G.; Armasu, I.; Bredetean, O.; Serban, I.; Preda, C. Protective role of selenium on thyroid morphology in iodine induced autoimmune thyroiditis in Wistar rats. Exp. Ther. Med., 2020, 20(4), 3425-3437.
[http://dx.doi.org/10.3892/etm.2020.9029] [PMID: 32905063]
[25]
Wang, W.; Zhang, B.T.; Jiang, Q.L.; Zhao, H.Q.; Xu, Q.; Zeng, Y.; Xu, J.Y.; Jiang, J. Leptin receptor antagonist attenuates experimental autoimmune thyroiditis in mice by regulating Treg/Th17 cell differentiation. Front. Endocrinol., 2022, 13, 1042511.
[http://dx.doi.org/10.3389/fendo.2022.1042511] [PMID: 36339447]
[26]
Cao, Y.; Jin, X.; Sun, Y.; Wen, W. Therapeutic effect of mesenchymal stem cell on Hashimoto’s thyroiditis in a rat model by modulating Th17/Treg cell balance. Autoimmunity, 2020, 53(1), 35-45.
[http://dx.doi.org/10.1080/08916934.2019.1697689] [PMID: 31793369]
[27]
Yi, H.; Tieshan, W.; Xiangyu, G.; Wen, S.; Xuan, G.; Lili, W.; Lingling, Q.; Chengfei, Z.; Tonghua, L. Protective effects of Jiayan Kangtai granules on autoimmune thyroiditis in a rat model by modulating Th17/Treg cell balance. J. Tradit. Chin. Med., 2018, 38(3), 380-390.
[http://dx.doi.org/10.1016/S0254-6272(18)30628-9] [PMID: 32185970]
[28]
Shao, S.; Yu, X.; Shen, L. Autoimmune thyroid diseases and Th17/Treg lymphocytes. Life Sci., 2018, 192, 160-165.
[http://dx.doi.org/10.1016/j.lfs.2017.11.026] [PMID: 29158050]
[29]
Mincer, D.L.; Jialal, I. Hashimoto Thyroiditis.StatPearls; StatPearls Publishing: Treasure Island, 2023.
[30]
Izic, B.; Custovic, A.; Caluk, S.; Fejzic, H.; Kundalic, B.; Husejnovic, M. The epidemiological characteristics of autoimmune thyroiditis in the tuzla canton in the period from 2015 to 2020. Mater. Sociomed., 2021, 33(4), 288-292.
[http://dx.doi.org/10.5455/msm.2021.33.288-292] [PMID: 35210952]
[31]
Klubo-Gwiezdzinska, J.; Wartofsky, L. Hashimoto thyroiditis: An evidence-based guide: etiology, diagnosis and treatment. Polish Arch. Intern. Med., 2022, 132(3), 16222.
[http://dx.doi.org/10.20452/pamw.16222] [PMID: 35243857]
[32]
Che, K.; Liu, X.; Chi, J.; Li, P.; Gao, J.; Fu, Z.; Yan, S.; Xing, X.; Hu, J. The effects of adipose-derived mesenchymal stem cells combined with sodium selenite on Hashimoto’s thyroiditis. Am. J. Transl. Res., 2020, 12(10), 6422-6433.
[PMID: 33194040]
[33]
Giammanco, M.; Giammanco, M.M. Selenium: A cure for autoimmune thyroiditis. Endocr. Metab. Immune Disord. Drug Targets, 2021, 21(8), 1377-1378.
[http://dx.doi.org/10.2174/1871530320666201014150147] [PMID: 33059572]
[34]
Wang, L.F.; Sun, R.X.; Li, C.F.; Wang, X.H. The effects of selenium supplementation on antibody titres in patients with Hashimoto’s thyroiditis. Endokrynol. Pol., 2021, 72(6), 666-667.
[http://dx.doi.org/10.5603/EP.a2021.0074] [PMID: 34378788]
[35]
Rayman, M.P. Multiple nutritional factors and thyroid disease, with particular reference to autoimmune thyroid disease. Proc. Nutr. Soc., 2019, 78(1), 34-44.
[http://dx.doi.org/10.1017/S0029665118001192] [PMID: 30208979]
[36]
Li, H.; Min, J.; Mao, X.; Wang, X.; Yang, Y.; Chen, Y. Edaravone ameliorates experimental autoimmune thyroiditis in rats through HO-1-dependent STAT3/PI3K/Akt pathway. Am. J. Transl. Res., 2018, 10(7), 2037-2046.
[PMID: 30093941]
[37]
Liu, H.; Tian, Q.; Ai, X.; Qin, Y.; Cui, Z.; Li, M.; Yang, J.; Zhai, D.; Liu, Y.; Chen, S.; Meng, J.; Sun, T.; Zhou, H.; Yang, C. Dihydroartemisinin attenuates autoimmune thyroiditis by inhibiting the CXCR3/PI3K/AKT/NF-kB signaling pathway. Oncotarget, 2017, 8(70), 115028-115040.
[http://dx.doi.org/10.18632/oncotarget.22854] [PMID: 29383139]
[38]
Wang, T.; Wang, Z.; Qi, W.; Jiang, G.; Wang, G. The role, targets and mechanisms of traditional Chinese medicine in regulating the balance of T helper type 17/regulatory Tcells in rheumatoid arthritis. Int. J. Rheum. Dis., 2023, 26(4), 613-624.
[http://dx.doi.org/10.1111/1756-185X.14560] [PMID: 36680325]
[39]
Xu, M.; Duan, X.Y.; Chen, Q.Y.; Fan, H.; Hong, Z.; Deng, S.J.; Nan, Z.; Wu, H.; Dong, Y.L.; Liu, Y.J.; Zhou, C.Z. Effect of compound sophorae decoction on dextran sodium sulfate (DSS)-induced colitis in mice by regulating Th17/Treg cell balance. Biomed. Pharmacother., 2019, 109, 2396-2408.
[http://dx.doi.org/10.1016/j.biopha.2018.11.087] [PMID: 30551499]
[40]
Xia, S.; Chen, L.; Li, Z.; Li, Y.; Zhou, Y.; Sun, S.; Su, Y.; Xu, X.; Shao, J.; Zhang, Z.; Kong, D.; Zhang, F.; Zheng, S. Qingchang wenzhong decoction reduce ulcerative colitis in mice by inhibiting Th17 lymphocyte differentiation. Phytomedicine, 2022, 107, 154460.
[http://dx.doi.org/10.1016/j.phymed.2022.154460] [PMID: 36182798]
[41]
Weetman, A.P. An update on the pathogenesis of Hashimoto’s thyroiditis. J. Endocrinol. Invest., 2021, 44(5), 883-890.
[http://dx.doi.org/10.1007/s40618-020-01477-1] [PMID: 33332019]
[42]
Vargas-Uricoechea, H. Molecular mechanisms in autoimmune thyroid disease. Cells, 2023, 12(6), 918.
[http://dx.doi.org/10.3390/cells12060918]
[43]
Ralli, M.; Angeletti, D.; Fiore, M.; D’Aguanno, V.; Lambiase, A.; Artico, M.; de Vincentiis, M.; Greco, A. Hashimoto’s thyroiditis: An update on pathogenic mechanisms, diagnostic protocols, therapeutic strategies, and potential malignant transformation. Autoimmun. Rev., 2020, 19(10), 102649.
[http://dx.doi.org/10.1016/j.autrev.2020.102649] [PMID: 32805423]
[44]
Kargar, M.; Torabizadeh, M.; Purrahman, D.; Zayeri, Z.D.; Saki, N. Regulatory factors involved in Th17/Treg cell balance of immune thrombocytopenia. Curr. Res. Transl. Med., 2023, 71(2), 103389.
[http://dx.doi.org/10.1016/j.retram.2023.103389] [PMID: 37062251]
[45]
Ma, R.; Su, H.; Jiao, K.; Liu, J. Role of Th17 cells, Treg cells, and Th17/Treg imbalance in immune homeostasis disorders in patients with chronic obstructive pulmonary disease. Immun. Inflamm. Dis., 2023, 11(2), e784.
[http://dx.doi.org/10.1002/iid3.784] [PMID: 36840492]
[46]
Huang, D.L.; He, Y.R.; Liu, Y.J.; He, H.Y.; Gu, Z.Y.; Liu, Y.M.; Liu, W.J.; Luo, Z.; Ju, M.J. The immunomodulation role of Th17 and Treg in renal transplantation. Front. Immunol., 2023, 14, 1113560.
[http://dx.doi.org/10.3389/fimmu.2023.1113560] [PMID: 36817486]
[47]
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]
[48]
He, X.; Liang, B.; Gu, N. Th17/Treg imbalance and atherosclerosis. Dis. Markers, 2020, 2020, 1-8.
[http://dx.doi.org/10.1155/2020/8821029] [PMID: 33193911]
[49]
Yang, X.; Chen, L.; Wang, S.; Wu, Y.; Zhou, X.; Meng, Z. The correlation between Th17/Treg immune dysregulation and the disease severity in chronic spontaneous urticaria patients. Immun. Inflamm. Dis., 2023, 11(7), e920.
[http://dx.doi.org/10.1002/iid3.920] [PMID: 37506162]
[50]
Lourenço, J.D.; Ito, J.T.; Martins, M.A.; Tibério, I.F.L.C.; Lopes, F.D.T.Q.S. Th17/Treg imbalance in chronic obstructive pulmonary disease: Clinical and experimental evidence. Front. Immunol., 2021, 12, 804919.
[http://dx.doi.org/10.3389/fimmu.2021.804919] [PMID: 34956243]
[51]
Hu, Y.; Feng, W.; Chen, H.; Shi, H.; Jiang, L.; Zheng, X.; Liu, X.; Zhang, W.; Ge, Y.; Liu, Y.; Cui, D. Effect of selenium on thyroid autoimmunity and regulatory T cells in patients with Hashimoto’s thyroiditis: A prospective randomized-controlled trial. Clin. Transl. Sci., 2021, 14(4), 1390-1402.
[http://dx.doi.org/10.1111/cts.12993] [PMID: 33650299]
[52]
Tian, X.; Li, N.; Su, R.; Dai, C.; Zhang, R. Selenium supplementation may decrease thyroid peroxidase antibody titer via reducing oxidative stress in euthyroid patients with autoimmune thyroiditis. Int. J. Endocrinol., 2020, 2020, 1-7.
[http://dx.doi.org/10.1155/2020/9210572] [PMID: 32676110]
[53]
Krysiak, R.; Kowalcze, K. Okopień, B. The impact of vitamin D on thyroid autoimmunity and hypothalamic–pituitary–thyroid axis activity in myo-inositol-treated and myo-inositol-naïve women with autoimmune thyroiditis: A pilot study. J. Clin. Pharm. Ther., 2022, 47(11), 1759-1767.
[http://dx.doi.org/10.1111/jcpt.13730] [PMID: 35775148]
[54]
Chahardoli, R.; Saboor-Yaraghi, A.A.; Amouzegar, A.; Khalili, D.; Vakili, A.; Azizi, F. Can supplementation with vitamin D modify thyroid autoantibodies (Anti-TPO Ab, Anti-Tg Ab) and thyroid profile (T3, T4, TSH) in hashimoto’s thyroiditis? A Double Blind, Randomized Clinical Trial. Horm. Metab. Res., 2019, 51(5), 296-301.
[http://dx.doi.org/10.1055/a-0856-1044] [PMID: 31071734]
[55]
Siddiq, A.; Naveed, A.K.; Ghaffar, N.; Aamir, M.; Ahmed, N. Association of pro-inflammatory cytokines with vitamin D in hashimoto’s thyroid autoimmune disease. Medicina (Kaunas), 2023, 59(5), 853.
[http://dx.doi.org/10.3390/medicina59050853] [PMID: 37241088]
[56]
Wang, W.; Jiang, Q.L.; Xu, Q.; Zeng, Y.; Jiang, R.; Jiang, J. Selenium regulates T cell differentiation in experimental autoimmune thyroiditis in mice. Int. Immunopharmacol., 2023, 28, 124.
[http://dx.doi.org/10.1016/j.intimp.2023.110993]
[57]
Chen, A.; Huang, L.; Zhang, L.; Helper, T. Correction: Helper T Cell 17 and Regulatory T cell levels in peripheral blood of newly diagnosed patients with autoimmune thyroid disease: A Meta-Analysis. Horm. Metab. Res., 2023, 55(1), e2.
[http://dx.doi.org/10.1055/a-2117-7652] [PMID: 36332627]
[58]
Fang, J.; Yu, L.; Zhuang, L.G.; Pei, X.Y.; Wang, Q.; Jin, G.X. The changes in peripheral blood Th17 and Treg ratios in Hashimoto’s thyroiditis are accompanied by differential PD-1/PD-L1 expression. Front. Endocrinol., 2022, 13, 959477.
[http://dx.doi.org/10.3389/fendo.2022.959477] [PMID: 36093111]
[59]
Cui, X.; Liu, Y.; Wang, S.; Zhao, N.; Qin, J.; Li, Y.; Fan, C.; Shan, Z.; Teng, W. Circulating exosomes activate dendritic cells and induce unbalanced CD4+ T cell differentiation in hashimoto thyroiditis. J. Clin. Endocrinol. Metab., 2019, 104(10), 4607-4618.
[http://dx.doi.org/10.1210/jc.2019-00273] [PMID: 31199456]
[60]
Scheinecker, C.; Göschl, L.; Bonelli, M. Treg cells in health and autoimmune diseases: New insights from single cell analysis. J. Autoimmun., 2020, 110, 102376.
[http://dx.doi.org/10.1016/j.jaut.2019.102376] [PMID: 31862128]
[61]
Vitales-Noyola, M.; Serrano-Somavilla, A.; Martínez-Hernández, R.; Sampedro-Nuñez, M.; Ramos-Levi, A.M.; González-Amaro, R.; Marazuela, M. Patients with autoimmune thyroiditis show diminished levels and defective suppressive function of Tr1 Regulatory. J. Clin. Endocrinol. Metab., 2018, 103(9), 3359-3367.
[http://dx.doi.org/10.1210/jc.2018-00498]
[62]
Gomez-Bris, R.; Saez, A.; Herrero-Fernandez, B.; Rius, C.; Sanchez-Martinez, H.; Gonzalez-Granado, J.M. CD4 T-Cell subsets and the pathophysiology of inflammatory bowel disease. Int. J. Mol. Sci., 2023, 24(3), 2696.
[http://dx.doi.org/10.3390/ijms24032696] [PMID: 36769019]
[63]
Wang, J.; Zhao, X.; Wan, Y.Y. Intricacies of TGF-β signaling in Treg and Th17 cell biology. Cell. Mol. Immunol., 2023, 20(9), 1002-1022.
[http://dx.doi.org/10.1038/s41423-023-01036-7] [PMID: 37217798]
[64]
Xu, H.; Wu, L.; Nguyen, H.H.; Mesa, K.R.; Raghavan, V.; Episkopou, V.; Littman, D.R. Arkadia-SKI/SnoN signaling differentially regulates TGF-β–induced iTreg and Th17 cell differentiation. J. Exp. Med., 2021, 218(11), e20210777.
[http://dx.doi.org/10.1084/jem.20210777] [PMID: 34473197]
[65]
Yan, J.; Luo, M.; Chen, Z.; He, B. The function and role of the Th17/Treg cell balance in inflammatory bowel disease. J. Immunol. Res., 2020, 2020, 1-8.
[http://dx.doi.org/10.1155/2020/8813558] [PMID: 33381606]
[66]
Motavalli, R.; Etemadi, J.; Soltani-Zangbar, M.S.; Ardalan, M.R.; Kahroba, H.; Roshangar, L.; Nouri, M.; Aghebati-Maleki, L.; Khiavi, F.M.; Abediazar, S.; Mehdizadeh, A.; Hojjat-Farsangi, M.; Mahmoodpoor, A.; Kafil, H.S.; Zolfaghari, M.; Ahmadian Heris, J.; Yousefi, M. Altered Th17/Treg ratio as a possible mechanism in pathogenesis of idiopathic membranous nephropathy. Cytokine, 2021, 141, 155452.
[http://dx.doi.org/10.1016/j.cyto.2021.155452] [PMID: 33571932]
[67]
Thomas, R.; Qiao, S.; Yang, X. Th17/Treg imbalance: Implications in lung inflammatory diseases. Int. J. Mol. Sci., 2023, 24(5), 4865.
[http://dx.doi.org/10.3390/ijms24054865] [PMID: 36902294]
[68]
Dang, E.V.; Barbi, J.; Yang, H.Y.; Jinasena, D.; Yu, H.; Zheng, Y.; Bordman, Z.; Fu, J.; Kim, Y.; Yen, H.R.; Luo, W.; Zeller, K.; Shimoda, L.; Topalian, S.L.; Semenza, G.L.; Dang, C.V.; Pardoll, D.M.; Pan, F. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell, 2011, 146(5), 772-784.
[http://dx.doi.org/10.1016/j.cell.2011.07.033] [PMID: 21871655]
[69]
Mao, Q.F.; Shang-Guan, Z.F.; Chen, H.L.; Huang, K. Immunoregulatory role of IL-2/STAT5/CD4+CD25+Foxp3 Treg pathway in the pathogenesis of chronic osteomyelitis. Ann. Transl. Med., 2019, 7(16), 384.
[http://dx.doi.org/10.21037/atm.2019.07.45] [PMID: 31555698]

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