Association of IL-13 rs20541 and rs1295686 variants with symptomatic asthma in a Saudi Arabian population

References

• Minty A, Chalon P, Derocq JM, Dumont X, Guillemot JC, Kaghad M, Labit C, Leplatois P, Liauzun P, Miloux B, et al. Interleukin-13 is a new human lymphokine regulating inflammatory and immune responses. Nature. 1993;362(6417):248–50.
   PubMed Web of Science ®Google Scholar
• Moy FJ, Diblasio E, Wilhelm J, Powers R. Solution structure of human IL-13 and implication for receptor binding. J Mol Biol. 2001;310(1):219–30.
   PubMed Web of Science ®Google Scholar
• Zhang JG, Hilton DJ, Willson TA, McFarlane C, Roberts BA, Moritz RL, Simpson RJ, Alexander WS, Metcalf D, Nicola NA. Identification, purification, and characterization of a soluble interleukin (IL)-13-binding protein. Evidence that it is distinct from the cloned Il-13 receptor and Il-4 receptor alpha-chains. J Biol Chem. 1997;272(14):9474–80.
   PubMed Web of Science ®Google Scholar
• Hershey GK. IL-13 receptors and signaling pathways: an evolving web. J Allergy Clin Immunol. 2003;111(4):677–60; quiz 691.
   PubMed Web of Science ®Google Scholar
• GeneCards. Human gene database. [ Last consultation 2017 Sep 25]. http://www.genecards.org/cgi-bin/carddisp.pl?gene = IL13.
   Google Scholar
• Tabata Y, Khurana Hershey GK. IL-13 receptor isoforms: breaking through the complexity. Curr Allergy Asthma Rep. 2007;7(5):338–45.
   PubMed Web of Science ®Google Scholar
• Burgos PI, Causey ZL, Tamhane A, Kelley JM, Brown EE, Hughes LB, Danila MI, van Everdingen A, Conn DL, Jonas BL, et al. Association of IL4R single-nucleotide polymorphisms with rheumatoid nodules in African Americans with rheumatoid arthritis. Arthr Res Ther. 2010;12(3):R75.
   PubMed Web of Science ®Google Scholar
• Zhang H, Lin L, Yang H, Zhang Z, Yang X, Zhang L, He S. Induction of IL-13 production and upregulation of gene expression of protease activated receptors in P815 cells by IL-6. Cytokine. 2010;50(2):138–45.
   PubMed Web of Science ®Google Scholar
• Liu Q, Liu Z, Whitmire J, Alem F, Hamed H, Pesce J, Urban JF Jr, Gause WC. IL-18 stimulates IL-13-mediated IFN-gamma-sensitive host resistance in vivo. Eur J Immunol. 2006;36(5):1187–98.
   PubMed Web of Science ®Google Scholar
• Toru H, Pawankar R, Ra C, Yata J, Nakahata T. Human mast cells produce IL-13 by high-affinity IgE receptor cross-linking: enhanced IL-13 production by IL-4-primed human mast cells. J Allergy Clin Immunol. 1998;102(3):491–502.
   PubMed Web of Science ®Google Scholar
• Medsger TA Jr, Ivanco DE, Kardava L, Morel PA, Lucas MR, Fuschiotti P. GATA-3 up-regulation in CD8+ T cells as a biomarker of immune dysfunction in systemic sclerosis, resulting in excessive interleukin-13 production. Arthr Rheum. 2011;63(6):1738–47.
   PubMed Web of Science ®Google Scholar
• Wilson S, Jones FM, Fofana HK, Landoure A, Kimani G, Mwatha JK, Sacko M, Vennervald BJ, Dunne DW. A late IL-33 response after exposure to Schistosoma haematobium antigen is associated with an up-regulation of IL-13 in human eosinophils. Parasite Immunol. 2013;35(7–8):224–8.
   PubMed Web of Science ®Google Scholar
• Zhang H, Yang H, Ma W, He S. Induction of IL-13 production and upregulated expression of protease activated receptor-1 by RANTES in a mast cell line. Cytokine. 2011;53(2):231–8.
   PubMed Web of Science ®Google Scholar
• Yashiro T, Kubo M, Ogawa H, Okumura K, Nishiyama C. PU.1 Suppresses Th2 cytokine expression via silencing of GATA3 transcription in dendritic cells. PLoS One. 2015;10(9):e0137699.
   PubMed Web of Science ®Google Scholar
• Shea-Donohue T, Sun R, Bohl JA, McLean LP, Zhao A. Enteric nematodes and the path to up-regulation of type 2 cytokines IL-4 and IL-13. Cytokine. 2015;75(1):62–7.
   PubMed Web of Science ®Google Scholar
• McDermott JR, Humphreys NE, Forman SP, Donaldson DD, Grencis RK. Intraepithelial NK cell-derived IL-13 induces intestinal pathology associated with nematode infection. J Immunol. 2005;175(5):3207–13.
   PubMed Web of Science ®Google Scholar
• Rutti S, Howald C, Arous C, Dermitzakis E, Halban PA, Bouzakri K. IL-13 improves beta-cell survival and protects against IL-1beta-induced beta-cell death. Mol Metab. 2016;5(2):122–31.
   PubMed Web of Science ®Google Scholar
• Tokayer A, Carsons SE, Chokshi B, Santiago-Schwarz F. High levels of interleukin 13 in rheumatoid arthritis sera are modulated by tumor necrosis factor antagonist therapy: association with dendritic cell growth activity. J Rheumatol. 2002;29(3):454–61.
   PubMed Web of Science ®Google Scholar
• Heitmann L, Abad Dar M, Schreiber T, Erdmann H, Behrends J, McKenzie AN, Brombacher F, Ehlers S, Holscher C. The IL-13/IL-4Rα axis is involved in tuberculosis-associated pathology. J Pathol. 2014;234(3):338–50.
   PubMed Web of Science ®Google Scholar
• Tomlinson KL, Davies GC, Sutton DJ, Palframan RT. Neutralisation of interleukin-13 in mice prevents airway pathology caused by chronic exposure to house dust mite. PLoS One. 2010;5(10):e13136.
   PubMed Web of Science ®Google Scholar
• Fulkerson PC, Fischetti CA, Hassman LM, Nikolaidis NM, Rothenberg ME. Persistent effects induced by IL-13 in the lung. Am J Respir Cell Mol Biol. 2006;35(3):337–46.
   PubMed Web of Science ®Google Scholar
• Alevy YG, Patel AC, Romero AG, Patel DA, Tucker J, Roswit WT, Miller CA, Heier RF, Byers DE, Brett TJ, et al. IL-13-induced airway mucus production is attenuated by MAPK13 inhibition. J Clin Investig. 2012;122(12):4555–68.
   PubMed Web of Science ®Google Scholar
• Lanone S, Zheng T, Zhu Z, Liu W, Lee CG, Ma B, Chen Q, Homer RJ, Wang J, Rabach LA, et al. Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and -12 in IL-13-induced inflammation and remodeling. J Clin Investig. 2002;110(4):463–74.
   PubMed Web of Science ®Google Scholar
• Lumsden RV, Worrell JC, Boylan D, Walsh SM, Cramton J, Counihan I, O'Beirne S, Medina MF, Gauldie J, Fabre A, et al. Modulation of pulmonary fibrosis by IL-13Rα2. Am J Physiol. Lung Cell Mol Physiol. 2015;308(7):L710–8.
   PubMed Web of Science ®Google Scholar
• Lachowicz-Scroggins ME, Boushey HA, Finkbeiner WE, Widdicombe JH. Interleukin-13-induced mucous metaplasia increases susceptibility of human airway epithelium to rhinovirus infection. Am J Respir Cell Mol Biol. 2010;43(6):652–61.
   PubMed Web of Science ®Google Scholar
• Tanabe T, Kanoh S, Tsushima K, Yamazaki Y, Kubo K, Rubin BK. Clarithromycin inhibits interleukin-13-induced goblet cell hyperplasia in human airway cells. Am J Respir Cell Mol Biol. 2011;45(5):1075–83.
   PubMed Web of Science ®Google Scholar
• Heinzmann A, Mao XQ, Akaiwa M, Kreomer RT, Gao PS, Ohshima K, Umeshita R, Abe Y, Braun S, Yamashita T, et al. Genetic variants of IL-13 signalling and human asthma and atopy. Hum Mol Genet. 2000;9(4):549–59.
   PubMed Web of Science ®Google Scholar
• Ramphul K, Hua L, Bao YX, Li JY, Liu QH, Ji RX, Fang DZ. Identification of IL13 C1923T as a single nucleotide polymorphism for asthma in children from Mauritius. Pediatr Allergy Immunol Pulmonol. 2015;28(2):92–5.
   PubMed Web of Science ®Google Scholar
• Vladich FD, Brazille SM, Stern D, Peck ML, Ghittoni R, Vercelli D. IL-13 R130Q, a common variant associated with allergy and asthma, enhances effector mechanisms essential for human allergic inflammation. J Clin Investig. 2005;115(3):747–54.
   PubMed Web of Science ®Google Scholar
• Battle NC, Choudhry S, Tsai HJ, Eng C, Kumar G, Beckman KB, Naqvi M, Meade K, Watson HG, Lenoir M, et al. Ethnicity-specific gene-gene interaction between IL-13 and IL-4Rα among African Americans with asthma. Am J Respir Critic Care Med. 2007;175(9):881–7.
   PubMed Web of Science ®Google Scholar
• Accordini S, Calciano L, Bombieri C, Malerba G, Belpinati F, Lo Presti AR, Baldan A, Ferrari M, Perbellini L, de Marco R. An Interleukin 13 polymorphism is associated with symptom severity in adult subjects with ever asthma. PLoS One. 2016;11(3):e0151292.
   PubMed Web of Science ®Google Scholar
• Liu Z, Li P, Wang J, Fan Q, Yan P, Zhang X, Han B. A meta-analysis of IL-13 polymorphisms and pediatric asthma risk. Med Sci Monit. 2014;20:2617–23.
   PubMed Web of Science ®Google Scholar
• Hakonarson H, Bjornsdottir US, Ostermann E, Arnason T, Adalsteinsdottir AE, Halapi E, Shkolny D, Kristjansson K, Gudnadottir SA, Frigge ML, et al. Allelic frequencies and patterns of single-nucleotide polymorphisms in candidate genes for asthma and atopy in Iceland. Am J Respir Critic Care Med. 2001; 164(11):2036–44.
   PubMed Web of Science ®Google Scholar
• Donfack J, Schneider DH, Tan Z, Kurz T, Dubchak I, Frazer KA, Ober C. Variation in conserved non-coding sequences on chromosome 5q and susceptibility to asthma and atopy. Respir Res. 2005;6:145.
   PubMed Web of Science ®Google Scholar
• Li X, Howard TD, Zheng SL, Haselkorn T, Peters SP, Meyers DA, Bleecker ER. Genome-wide association study of asthma identifies RAD50-IL13 and HLA-DR/DQ regions. J Allergy Clin Immunol. 2010;125(2):328–35.e11.
   PubMed Web of Science ®Google Scholar
• Liu Y, Liu T, Nie W, Lai G, Xiu Q. Interleukin-13 +1923C/T polymorphism is associated with asthma risk: a meta-analysis. BioMed Res Int. 2013;2013:394316.
   PubMed Web of Science ®Google Scholar
• Cui L, Jia J, Ma CF, Li SY, Wang YP, Guo XM, Li Q, Yu HB, Liu WH, Gao LB. IL-13 polymorphisms contribute to the risk of asthma: a meta-analysis. Clin Biochem. 2012;45(4–5):285–8.
   PubMed Web of Science ®Google Scholar
• Hunninghake GM, Soto-Quiros ME, Avila L, Su J, Murphy A, Demeo DL, Ly NP, Liang C, Sylvia JS, Klanderman BJ, et al. Polymorphisms in IL13, total IgE, eosinophilia, and asthma exacerbations in childhood. J Allergy Clin Immunol. 2007;120(1):84–90.
   PubMed Web of Science ®Google Scholar
• Tsai CH, Tung KY, Su MW, Chiang BL, Chew FT, Kuo NW, Lee YL. Interleukin-13 genetic variants, household carpet use and childhood asthma. PLoS One. 2013;8(1):e51970.
   PubMed Web of Science ®Google Scholar
• Adjers K, Luukkainen A, Pekkanen J, Hurme M, Huhtala H, Renkonen R, Wang Y, Makela MJ, Karjalainen J, Toppila-Salmi S. Self-reported allergic rhinitis and/or allergic conjunctivitis associate with IL13 rs20541 polymorphism in Finnish adult asthma patients. Int Arch Allergy Immunol. 2017;172(2):123–8.
   PubMed Web of Science ®Google Scholar
• Al-Muhsen S, Vazquez-Tello A, Jamhawi A, Al-Dosari MS, Mahboub B, Iqbal N, Temsah MH, Al-Eyadhy A, Alharbi N, Halwani R. Rs37972 and rs37973 single-nucleotide polymorphisms in the glucocorticoid-inducible 1 gene are not associated with asthma risk in a Saudi Arabian population. J Asthma. 2015;52(2):115–22.
   PubMed Web of Science ®Google Scholar
• Bateman ED, Hurd SS, Barnes PJ, Bousquet J, Drazen JM, FitzGerald M, Gibson P, Ohta K, O'Byrne P, Pedersen SE, et al. Global strategy for asthma management and prevention: GINA executive summary. Eur Respir J. 2008;31(1):143–78.
   PubMed Web of Science ®Google Scholar
• Graves PE, Kabesch M, Halonen M, Holberg CJ, Baldini M, Fritzsch C, Weiland SK, Erickson RP, von Mutius E, Martinez FD. A cluster of seven tightly linked polymorphisms in the IL-13 gene is associated with total serum IgE levels in three populations of white children. J Allergy Clin Immunol. 2000;105(3):506–13.
   PubMed Web of Science ®Google Scholar
• Al-Muhsen S, Vazquez-Tello A, Alzaabi A, Al-Hajjaj MS, Al-Jahdali HH, Halwani R. IL-4 receptor alpha single-nucleotide polymorphisms rs1805010 and rs1801275 are associated with increased risk of asthma in a Saudi Arabian population. Ann Thorac Med. 2014;9(2):81–6.
   PubMed Web of Science ®Google Scholar
• Halwani R, Vazquez-Tello A, Horanieh N, Dulgom S, Al-Aseri Z, Al-Khamis N, Al-Sum Z, Al-Jahdali H, Al-Muhsen S. Risk factors hindering asthma symptom control in Saudi children and adolescents. Pediatr Int. 2017;59(6):661–8.
   PubMed Web of Science ®Google Scholar
• Sole X, Guino E, Valls J, Iniesta R, Moreno V. SNPStats: a web tool for the analysis of association studies. Bioinformatics. 2006;22(15):1928–9.
   PubMed Web of Science ®Google Scholar
• Bland JM, Altman DG. Statistics notes. The odds ratio. BMJ. 2000;320(7247):1468.
   PubMed Web of Science ®Google Scholar
• Tan HT, Sugita K, Akdis CA. Novel biologicals for the treatment of allergic diseases and asthma. Curr Allergy Asthma Rep. 2016;16(10):70.
   PubMed Web of Science ®Google Scholar
• Bagnasco D, Ferrando M, Varricchi G, Passalacqua G, Canonica GW. A critical evaluation of anti-IL-13 and Anti-IL-4 strategies in severe asthma. Int Arch Allergy Immunol. 2016;170(2):122–31.
   PubMed Web of Science ®Google Scholar
• Andiappan AK, Rotzschke O, Wang de Y, Chew FT. Association of interleukin-13 SNP rs20541 (Arg>Gln) to allergic rhinitis in an Asian population of ethnic Chinese in Singapore. Gene. 2013;529(2):357–8.
   PubMed Web of Science ®Google Scholar
• Tantisira KG, Lasky-Su J, Harada M, Murphy A, Litonjua AA, Himes BE, Lange C, Lazarus R, Sylvia J, Klanderman B, et al. Genomewide association between GLCCI1 and response to glucocorticoid therapy in asthma. New Engl J Med. 2011;365(13):1173–83.
   PubMed Web of Science ®Google Scholar
• Schieck M, Sharma V, Michel S, Toncheva AA, Worth L, Potaczek DP, Genuneit J, Kretschmer A, Depner M, Dalphin JC, et al. A polymorphism in the TH 2 locus control region is associated with changes in DNA methylation and gene expression. Allergy. 2014;69(9):1171–80.
   PubMed Web of Science ®Google Scholar
• Ober C. Asthma genetics in the post-GWAS era. Ann Am Thorac Soc. 2016;13(Suppl 1):S85–90.
   PubMed Web of Science ®Google Scholar
• Weidinger S, Willis-Owen SA, Kamatani Y, Baurecht H, Morar N, Liang L, Edser P, Street T, Rodriguez E, O'Regan GM, et al. A genome-wide association study of atopic dermatitis identifies loci with overlapping effects on asthma and psoriasis. Hum Mol Genet. 2013;22(23):4841–56.
   PubMed Web of Science ®Google Scholar
• Utsumi Y, Sasaki N, Nagashima H, Suzuki N, Nakamura Y, Yamashita M, Kobayashi H, Yamauchi K. Association of IL-13 gene polymorphisms with airway hyperresponsiveness in a Japanese adult asthmatic population. Respir Invest. 2013;51(3):147–52.
   PubMedGoogle Scholar
• Narozna B, Hoffmann A, Sobkowiak P, Schoneich N, Breborowicz A, Szczepankiewicz A. Polymorphisms in the interleukin 4, interleukin 4 receptor and interleukin 13 genes and allergic phenotype: a case control study. Adv Med Sci. 2016;61(1):40–5.
   PubMed Web of Science ®Google Scholar
• Alasandagutti ML, Ansari MS, Sagurthi SR, Valluri V, Gaddam S. Role of IL-13 genetic variants in signalling of asthma. Inflammation. 2017;40(2):566–77.
   PubMed Web of Science ®Google Scholar
• Resende EP, Todo-Bom A, Loureiro C, Mota Pinto A, Oliveiros B, Mesquita L, Silva HC. Asthma and rhinitis have different genetic profiles for IL13, IL17A and GSTP1 polymorphisms. Rev Port Pneumol (2006). 2017;23(1):10–16.
   PubMed Web of Science ®Google Scholar
• Li T, Ren Z, Deng Y, Wang Y, Zhou H. Lack of association between RAD50-IL13 polymorphisms and pediatric asthma susceptibility in Northeastern Han Chinese. J Asthma. 2016;53(2):114–8.
   PubMed Web of Science ®Google Scholar
• Long X, Chen Q, Zhao J, Rafaels N, Mathias P, Liang H, Potee J, Campbell M, Zhang B, Gao L, et al. An IL-13 promoter polymorphism associated with liver fibrosis in patients with Schistosoma japonicum. PLoS One. 2015;10(8):e0135360.
   PubMed Web of Science ®Google Scholar
• Ellis MK, Zhao ZZ, Chen HG, Montgomery GW, Li YS, McManus DP: Analysis of the 5q31 33 locus shows an association between single nucleotide polymorphism variants in the IL-5 gene and symptomatic infection with the human blood fluke, Schistosoma japonicum. J Immunol. 2007;179(12):8366–71.
   PubMed Web of Science ®Google Scholar
• Nie W, Liu Y, Bian J, Li B, Xiu Q. Effects of polymorphisms -1112C/T and +2044A/G in interleukin-13 gene on asthma risk: a meta-analysis. PLoS One. 2013;8(2):e56065.
   PubMed Web of Science ®Google Scholar
• Patil VK, Holloway JW, Zhang H, Soto-Ramirez N, Ewart S, Arshad SH, Karmaus W. Interaction of prenatal maternal smoking, interleukin 13 genetic variants and DNA methylation influencing airflow and airway reactivity. Clin Epigenet. 2013;5(1):22.
   PubMed Web of Science ®Google Scholar
• Maier LM, Chapman J, Howson JM, Clayton DG, Pask R, Strachan DP, McArdle WL, Twells RC, Todd JA. No evidence of association or interaction between the IL4RA, IL4, and IL13 genes in type 1 diabetes. Am J Hum Genet. 2005;76(3):517–21.
   PubMed Web of Science ®Google Scholar
• Granada M, Wilk JB, Tuzova M, Strachan DP, Weidinger S, Albrecht E, Gieger C, Heinrich J, Himes BE, Hunninghake GM, et al. A genome-wide association study of plasma total IgE concentrations in the Framingham Heart Study. J Allergy Clin Immunol. 2012;129(3):840–5.e21.
   PubMed Web of Science ®Google Scholar
• Ashley SE, Tan HT, Peters R, Allen KJ, Vuillermin P, Dharmage SC, Tang MLK, Koplin J, Lowe A, Ponsonby AL, et al. Genetic variation at the Th2 immune gene IL13 is associated with IgE-mediated paediatric food allergy. Clin Exp Allergy. 2017;47(8):1032–7.
   PubMed Web of Science ®Google Scholar
• Berulava T, Horsthemke B. The obesity-associated SNPs in intron 1 of the FTO gene affect primary transcript levels. Eur J Hum Genet. 2010;18(9):1054–6.
   PubMed Web of Science ®Google Scholar