Interleukin-10 Promoter 1082/−819/−592 Polymorphisms are Associated with Asthma Susceptibility in Asians and Atopic Asthma: A Meta-Analysis

Xue-yan Zheng1, Wei-jie Guan2, Chen Mao3, Hui-fang Chen1, Hong Ding1, Jin-ping Zheng2, Ting-ting Hu1, Min-hong Luo1, Yan-hui Huang1, Qing Chen1
1Department of Epidemiology, School of Public Health and Tropical Medicine, Southern Medical University, Guangzhou, China
2State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, China
3Division of Epidemiology, School of Public Health and Primary Care, The Chinese University of Hong Kong, Shatin, Hong Kong SAR, China

Tóm tắt

Although interleukin-10 (IL-10) is a potent inhibitor of allergic diseases, the association between promoter −1082/−819/−592 polymorphisms and asthma susceptibility remains inconclusive. We sought to determine if IL-10 promoter −1082/−819/−592 polymorphisms contribute to asthma susceptibility and are associated with phenotypes of atopic asthma. Systematic computerized searches were performed. Pooled odds ratios (ORs) and 95 % confidence intervals (CIs) were estimated by using random-effect and fixed-effect models, based on between-study heterogeneity. Subgroup analyses were performed according to age, ethnicity, and atopy. Publication bias was detected by funnel plot using Egger’s test. A total of 4,716 asthmatic patients and 5,093 controls were included. The asthma susceptibility correlated significantly with IL-10 promoter gene −1082 polymorphism [OR (95 % CI) 1.26 (1.02, 1.55) for AA vs. AG + GG] and −592 polymorphism [OR (95 % CI) 1.12 (1.07, 1.34) for AC + AA vs. CC] (both P < 0.05), but not with −819 polymorphism (P > 0.05). Subgroup analyzes suggested that the AA versus AG + GG genotype of −1082A/G polymorphism and AC + AA versus CC genotype of −592A/C polymorphism contributed significantly to increased asthma susceptibility in adults [OR (95 % CI) 1.39 (1.03, 1.87) for −1082A/G and 1.53 (1.25, 1.87) for −592A/C polymorphism]. The Asian population [OR (95 % CI) 1.35 (1.1, 1.7) for −1082A/G and 1.4 (1.12, 1.64) for −592A/C polymorphism] and subjects with atopic asthma [OR (95 % CI) 1.49 (1.18, 1.88) for −1082A/G and 1.23 (1.01, 1.48) for −592A/C polymorphism] also had an increased susceptibility of asthma. No publication bias was detected. IL-10 promoter −1028A/G, −592A/C polymorphisms and their haplotypes, but not −819T/C polymorphism, correlate with asthma susceptibility.

Tài liệu tham khảo

Sobande PO, Kercsmar CM (2008) Inhaled corticosteroids in asthma management. Respir Care 53(5):625–633 Busse WW, Lemanske RF (2001) Asthma. N Engl J Med 344(5):350–362 Magnan AO, Mely LG, Camilla CA, Badier MM, Montero-Julian FA (2000) Assessment of the Th1/Th2 paradigm in whole blood in atopy and asthma. Increased IFN-gamma-producing CD8+ T cells in asthma. Am J Respir Crit Care Med 161:1790–1796 Barnes PJ (2001) IL-10: a key regulator or allergic disease. Curr Opin Allergy Clin Immunol 31:667–669 Taga K, Tosato G (1992) IL-10 inhibits human T cell proliferation and IL-2 production. J Immunol 148:1143–1148 Barnes PJ (1998) Inhibitory cytokines in asthma. Mol Med Today 4:452–458 Karjalainen J, Hulkkonen J, Nieminen MM, Huhtala H, Aromaa A, Klaukka T et al (2003) Interleukin-10 gene promoter region polymorphism is associated with eosinophil count and circulating immunoglobulin E in adult asthma. Clin Exp Allergy 33:78–83 Chatterjee R, Batra J, Kumar A (2005) Interleukin-10 promoter polymorphisms and atopic asthma in North Indians. Clin Exp Allergy 35:914–919 Li ZF, Lu JH, Li JR, Liao BP (2007) Lack of association between children asthma and interleukin-10 polymorphism. Cent Plains Med J 34(14):4–5 Trajkov D, Stojkovikj JM, Arsov T, Petlichkovski A, Strezova A, Efinska-Mladenovska O et al (2008) Association of cytokine gene polymorphisms with bronchial asthma in Macedonians. Iran J Allergy Asthma Immunol 7:143–156 Kim KW, Lee KE, Hong JY (2011) Involvement of IL-10 gene promoter polymorphisms in the susceptibility for childhood asthma. Lung 189:417–423 Lim S, Crawley E, Woo P, Barnes PJ (1998) Haplotype associated with low interleukin-10 production in patients with severe asthma. Lancet 352:113 Schubert K, Von Bonnsdorf H, Burke M, Ahlert I, Braun S, Berner R et al (2006) A comprehensive candidate gene study on bronchial asthma and juvenile idiopathic arthritis. Dis Markers 22:127–132 Hákonarson H, Bjornsdottir US, Ostermann E, Arnason T, Adalsteinsdottir AE, Halapi E et al (2001) Allelic frequencies and patterns of single nucleotide polymorphisms in candidate genes for asthma and atopy in Iceland. Am J Respir Crit Care Med 164:2036–2044 Daley D, Lemire M, Akhabir L, Chan-Yeung M, He JQ, McDonald T et al (2009) Analyses of associations with asthma in four asthma population samples from Canada and Australia. Hum Genet 125:445–459 Zedan M, Settin A, Farag MK, El-Bayoumi M, Regal E, El Baz R et al (2008) Gene polymorphisms of tumor necrosis factor alpha-308 and interleukin-10-1082 among asthmatic Egyptian children. Allergy Asthma Proc 29:268–273 Movahedi M, Mahdaviani SA, Rezaei N, Moradi B, Dorkhosh S, Amirzargar AA (2008) IL-10, TGF-β, IL-2, IL-12 and IFN-γ cytokine gene polymorphisms in asthma. J Asthma 45:790–794 Xie Q (2012) Study of the correlation between IL-10 gene −627C/A polymorphism and childhood asthma. Xian Dai Yi Xue 40(1):51–53 Hang LW, Hsia TC, Chen WC, Chen HY, Tsai JJP, Tsai FJ et al (2003) Interleukin-10 gene −627 allele variants, not interleukin-I beta gene and receptor antagonist gene polymorphisms, are associated with atopic bronchial asthma. J Clin Lab Anal 17:168–173 Park BL, Kim LH, Choi YH, Lee JH, Rhim T, Lee YM et al (2004) Interleukin 3 (IL-3) polymorphisms associated with decreased risk of asthma and atopy. J Hum Genet 49:517–527 Li HL, Zhao XF, Huang YK (2006) A study on association between the interleukin-10 −627 (C/A) polymorphism and childhood asthma. Zhongguo You Sheng Yu Yi Chuan Za Zhi 14:15–17 Yang XX, Li FX, Li X, Sun JZ, Sun MY, Li M (2010) Association of single nucleotide polymorphisms in interleukin-10 gene with asthma. Chin J Respir Crit Care Med 9(5):485–489 Hakimizadeh E, Arababadi MK, Hassanshaihi G, Ahmadabadi BN, Hassanshahi G, Ahmadabadi BN et al (2012) Association of −592 region of IL-10 polymorphisms with asthma in south-eastern Iranian patients. Clin Lab 58:267–271 Hussein YM, Shalaby SM, Mohamed RH, Hassan TH (2011) Association between genes encoding components of the IL-10/IL-0 receptor pathway and asthma in children. Ann Allergy Asthma Immunol 106:474–480 Undarmaa S, Mashimo Y, Hattori S, Shimojo N, Fujita K, Miyatake A et al (2010) Replication of genetic association studies in asthma and related phenotypes. J Hum Genet 55:342–349 Ji X, Jia SD, Zhang WZ, Wang HY, Wang XX, Li J et al (2011) Association between polymorphism of interleukin-10 gene promoter and susceptibility to atopic asthma. Xian Dai Sheng Wu Xue Jin Zhan 11:3041–3044 Yu FF, Guan LX, Ji JF, Liu CY, Jia N, Li HL (2011) Study about association of IL-10 gene −592 C/A polymorphism with bronchial asthma in children. Wei Fang Yi Xue Yuan Xue Bao 33(4):279–282 Xing F, Jiang YX, Liu WY, Li CP, Wang Y (2012) Studies on association between IL-10 gene promoter polymorphisms and asthma Han nationality from Wannan area in Anhui province. Zhong Guo Mian Yi Xue Za Zhi 28:624–630 Nie W, Fang Z, Li B, Xiu QY et al (2012) Interleukin-10 promoter polymorphisms and asthma risk: a meta-analysis. Cytokine 60(3):849–855 Hyun MH, Lee CH, Kang MH, Park BK, Lee YH (2013) Interleukin-10 promoter gene polymorphisms and susceptibility to asthma: a meta-analysis. PLoS ONE 8(1):e53758 Thakkinstian A, McElduff P, D’Este C, Duffy D, Attia J (2005) A method for meta-analysis of molecular association studies. Stat Med 24:1291–1306 Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560 Hardy RJ, Thompsom SG (1998) Detecting and describing heterogeneity in meta-analysis. Stat Med 17:841–856 DerSimonian R, Laird N (1998) Meta-analysis in clinical trials. Control Clin Trials 7:177–188 Lyon H, Lange C, Lake S, Silverman EK, Randolph AG et al (2004) IL-10 gene polymorphisms are associated with asthma phenotypes in children. Genet Epidemiol 26:155–165 Akdis M, Akdis CA (2009) Therapeutic manipulation of immune tolerance in allergic disease. Nat Rev Drug Discov 8:645–660 Borish L (1998) Updates on cells and cytokines. J Allergy Clin Immunol 101:293–297 Prasse A, Germann M, Pechkovsky DV, Markert A, Verres T, Stahl M et al (2006) IL-10-producing monocytes differentiate to alternatively activated macrophages and are increased in atopic patients. J Allergy Clin Immunol 119:464–471 Hobbs K, Negri J, Klinnert M, Rosenwasser LJ, Borish L (1998) Interleukin-10 and transforming growth factor-β promoter polymorphisms in allergies and asthma. Am J Respir Crit Care Med 158:1958–1962 Karjalainen J, Virta M, Pessi T, Hulkkonen J, Nieminen MM, Hurme M et al (2005) Childhood cat exposure related tolerance is associated with IL-1a and IL-10 polymorphisms. J Allergy Clin Immunol 116:223–225 Wacholder S, Chanock S, Garcia-Closas M, El Ghormli L, Rothman N (2004) Assessing the probability that a positive report is false: an approach for molecular epidemiology studies. J Natl Cancer Inst 96:434–442