TIM4-TIM1 interaction modulates Th2 pattern inflammation through enhancing SIRT1 expression

Hu,Tianyong; Fan,Xiaoqin; Ma,Li; Liu,Jiangqi; Chang,Yunli; Yang,Pingchang; Qiu,Shuqi; Chen,Tao; Yang,Litao; Liu,Zhiqiang

doi:10.3892/ijmm.2017.3150

TIM4-TIM1 interaction modulates Th2 pattern inflammation through enhancing SIRT1 expression

Authors:
- Tianyong Hu
- Xiaoqin Fan
- Li Ma
- Jiangqi Liu
- Yunli Chang
- Pingchang Yang
- Shuqi Qiu
- Tao Chen
- Litao Yang
- Zhiqiang Liu
View Affiliations

Affiliations: Immunology and Allergy Laboratory, Longgang ENT Hospital, Institute of ENT and Shenzhen Key Laboratory of ENT, Shenzhen, Guangdong 518172, P.R. China, Department of Gastroenterology, Shanghai Pudong New Area Zhoupu Hospital, Shanghai 201318, P.R. China, Shenzhen Key Laboratory of Allergy and Immunology, Shenzhen University School of Medicine and State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen, Guangdong 518060, P.R. China
Published online on: September 25, 2017 https://doi.org/10.3892/ijmm.2017.3150
Pages: 1504-1510
Copyright: © Hu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Skewed T helper 2 (Th2)‑cell polarization plays a critical role in the pathogenesis of allergic inflammations; however, the underlying mechanisms require further elucidation. The aim of the present study was to investigate the mechanisms through which the interaction between T‑cell immunoglobulin and mucin domain (TIM)4 and TIM1 regulates the expression of silent information regulator 1 (SIRT1) in Th2 cells, and the role of SIRT1 in Th2‑cell polarization during nasal allergic inflammation. The results demonstrated that TIM4 expression by splenic dendritic cells was increased in mice with allergic rhinitis, and the TIM4̸TIM1 interaction promoted CD4+ T cells to express SIRT1 during allergic inflammation via enhancing phosphoinositide 3‑kinase/Akt phosphorylation. SIRT1 then facilitated CD4+ T‑cell proliferation through downregulating the expression of Fas ligand, caspase-3 and p53 in mice with nasal allergic inflammation. In conclusion, the interaction of TIM4̸TIM1 was found to promote Th2‑cell proliferation through enhancing SIRT1 expression in mice with nasal allergic rhinitis.

View Figures

View References

1	Sicherer SH and Sampson HA: Food allergy: Epidemiology, pathogenesis, diagnosis, and treatment. J Allergy Clin Immunol. 133:291–307; quiz 308. 2014. View Article : Google Scholar : PubMed/NCBI
2	Heratizadeh A: Atopic dermatitis: New evidence on the role of allergic inflammation. Curr Opin Allergy Clin Immunol. 16:458–464. 2016. View Article : Google Scholar : PubMed/NCBI
3	Rosati MG and Peters AT: Relationships among allergic rhinitis, asthma, and chronic rhinosinusitis. Am J Rhinol Allergy. 30:44–47. 2016. View Article : Google Scholar : PubMed/NCBI
4	Eifan AO and Durham SR: Pathogenesis of rhinitis. Clin Exp Allergy. 46:1139–1151. 2016. View Article : Google Scholar : PubMed/NCBI
5	Oettgen HC and Burton OT: IgE receptor signaling in food allergy pathogenesis. Curr Opin Immunol. 36:109–114. 2015. View Article : Google Scholar : PubMed/NCBI
6	Hiraishi Y, Nambu A, Shibui A, Nakanishi W, Yamaguchi S, Morita H, Iikura M, McKenzie AN, Matsumoto K, Sudo K, et al: TIM-3 is not essential for development of airway inflammation induced by house dust mite antigens. Allergol Int. 65:459–465. 2016. View Article : Google Scholar : PubMed/NCBI
7	Li Z, Ju Z and Frieri M: The T-cell immunoglobulin and mucin domain (Tim) gene family in asthma, allergy, and autoimmunity. Allergy Asthma Proc. 34:e21–e26. 2013. View Article : Google Scholar : PubMed/NCBI
8	Freeman GJ, Casasnovas JM, Umetsu DT and DeKruyff RH: TIM genes: A family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol Rev. 235:172–189. 2010. View Article : Google Scholar : PubMed/NCBI
9	Feng BS, Chen X, He SH, Zheng PY, Foster J, Xing Z, Bienenstock J and Yang PC: Disruption of T-cell immunoglobulin and mucin domain molecule (TIM)-1/TIM4 interaction as a therapeutic strategy in a dendritic cell-induced peanut allergy model. J Allergy Clin Immunol. 122:55–61. e1–7. 2008. View Article : Google Scholar : PubMed/NCBI
10	Santiago C, Ballesteros A, Tami C, Martínez-Muñoz L, Kaplan GG and Casasnovas JM: Structures of T Cell immunoglobulin mucin receptors 1 and 2 reveal mechanisms for regulation of immune responses by the TIM receptor family. Immunity. 26:299–310. 2007. View Article : Google Scholar : PubMed/NCBI
11	Binne LL, Scott ML and Rennert PD: Human TIM-1 associates with the TCR complex and up-regulates T cell activation signals. J Immunol. 178:4342–4350. 2007. View Article : Google Scholar : PubMed/NCBI
12	Haigis MC and Sinclair DA: Mammalian sirtuins: Biological insights and disease relevance. Annu Rev Pathol. 5:253–295. 2010. View Article : Google Scholar : PubMed/NCBI
13	Wang Y, Li D, Ma G, Li W, Wu J, Lai T, Huang D, Zhao X, Lv Q, Chen M, et al: Increases in peripheral SIRT1: A new biological characteristic of asthma. Respirology. 20:1066–1072. 2015. View Article : Google Scholar : PubMed/NCBI
14	Colley T, Mercado N, Kunori Y, Brightling C, Bhavsar PK, Barnes PJ and Ito K: Defective sirtuin-1 increases IL-4 expression through acetylation of GATA-3 in patients with severe asthma. J Allergy Clin Immunol. 137:1595–1597.e7. 2016. View Article : Google Scholar
15	Legutko A1, Marichal T, Fiévez L, Bedoret D, Mayer A, de Vries H, Klotz L, Drion PV, Heirman C, Cataldo D, et al: Sirtuin 1 promotes Th2 responses and airway allergy by repressing peroxisome proliferator-activated receptor-gamma activity in dendritic cells. J Immunol. 187:4517–4529. 2011. View Article : Google Scholar : PubMed/NCBI
16	Kim YH, Yang TY, Park CS, Ahn SH, Son BK, Kim JH, Lim DH and Jang TY: Anti-IL-33 antibody has a therapeutic effect in a murine model of allergic rhinitis. Allergy. 67:183–190. 2012. View Article : Google Scholar
17	de Souza AJ, Oriss TB, O'malley KJ, Ray A and Kane LP: T cell Ig and mucin 1 (TIM-1) is expressed on in vivo-activated T cells and provides a costimulatory signal for T cell activation. Proc Natl Acad Sci USA. 102:17113–17118. 2005. View Article : Google Scholar : PubMed/NCBI
18	Li J, Zhao X, Liu X and Liu H: Disruption of TIM-4 in dendritic cell ameliorates hepatic warm IR injury through the induction of regulatory T cells. Mol Immunol. 66:117–125. 2015. View Article : Google Scholar : PubMed/NCBI
19	Sonar SS, Hsu YM, Conrad ML, Majeau GR, Kilic A, Garber E, Gao Y, Nwankwo C, Willer G, Dudda JC, et al: Antagonism of TIM-1 blocks the development of disease in a humanized mouse model of allergic asthma. J Clin Invest. 120:2767–2781. 2010. View Article : Google Scholar : PubMed/NCBI
20	Kim HY, Chang YJ, Chuang YT, Lee HH, Kasahara DI, Martin T, Hsu JT, Savage PB, Shore SA, Freeman GJ, et al: T-cell immunoglobulin and mucin domain 1 deficiency eliminates airway hyperreactivity triggered by the recognition of airway cell death. J Allergy Clin Immunol. 132:414–425.e6. 2013. View Article : Google Scholar : PubMed/NCBI
21	Yeung MY, McGrath M and Najafian N: The emerging role of the TIM molecules in transplantation. Am J Transplant. 11:2012–2019. 2011. View Article : Google Scholar : PubMed/NCBI
22	Mariat C, Degauque N, Balasubramanian S, Kenny J, DeKruyff RH, Umetsu DT, Kuchroo V, Zheng XX and Strom TB: Tim-1 signaling substitutes for conventional signal 1 and requires costimulation to induce T cell proliferation. J Immunol. 182:1379–1385. 2009. View Article : Google Scholar : PubMed/NCBI
23	de Souza AJ, Oak JS, Jordanhazy R, DeKruyff RH, Fruman DA and Kane LP: T cell Ig and mucin domain-1-mediated T cell activation requires recruitment and activation of phosphoinositide 3-kinase. J Immunol. 180:6518–6526. 2008. View Article : Google Scholar : PubMed/NCBI
24	Koga T, Suico MA, Shimasaki S, Watanabe E, Kai Y, Koyama K, Omachi K, Morino-Koga S, Sato T, Shuto T, et al: Endoplasmic reticulum (ER) stress induces sirtuin 1 (SIRT1) expression via the PI3K-Akt-GSK3β signaling pathway and promotes hepato-cellular injury. J Biol Chem. 290:30366–30374. 2015. View Article : Google Scholar : PubMed/NCBI
25	Ming GF, Tang YJ, Hu K, Chen Y, Huang WH and Xiao J: Visfatin attenuates the ox-LDL-induced senescence of endothelial progenitor cells by upregulating SIRT1 expression through the PI3K/Akt/ERK pathway. Int J Mol Med. 38:643–649. 2016. View Article : Google Scholar : PubMed/NCBI
26	Kim SR, Lee KS, Park SJ, Min KH, Choe YH, Moon H, Yoo WH, Chae HJ, Han MK and Lee YC: Involvement of sirtuin 1 in airway inflammation and hyperresponsiveness of allergic airway disease. J Allergy Clin Immunol. 125:449–460.e14. 2010. View Article : Google Scholar
27	Tanno M, Sakamoto J, Miura T, Shimamoto K and Horio Y: Nucleocytoplasmic shuttling of the NAD⁺-dependent histone deacetylase SIRT1. J Biol Chem. 282:6823–6832. 2007. View Article : Google Scholar : PubMed/NCBI
28	Arakaki R, Yamada A, Kudo Y, Hayashi Y and Ishimaru N: Mechanism of activation-induced cell death of T cells and regulation of FasL expression. Crit Rev Immunol. 34:301–314. 2014. View Article : Google Scholar : PubMed/NCBI
29	Porter AG and Jänicke RU: Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6:99–104. 1999. View Article : Google Scholar : PubMed/NCBI
30	Yang L, Xu LZ, Liu ZQ, Yang G, Geng XR, Mo LH, Liu ZG, Zheng PY and Yang PC: Interleukin-13 interferes with activation-induced T-cell apoptosis by repressing p53 expression. Cell Mol Immunol. 13:669–677. 2016. View Article : Google Scholar :