Inflammatory and Immune Response Genes Polymorphisms are Associated with Susceptibility to Chronic Obstructive Pulmonary Disease in Tatars Population from Russia

Biochemical Genetics volume 54, pages 388–412 (2016)Cite this article

Abstract

Chronic obstructive pulmonary disease (COPD) is a complex chronic inflammatory disease of the respiratory system affecting primarily distal respiratory pathways and lung parenchyma. This work was designed as a case–control study aimed at investigating the association of COPD with polymorphisms in inflammatory and immune response genes (JAK1, JAK3, STAT1, STAT3, NFKB1, IL17A, ADIPOQ, ADIPOR1, etc.) in Tatar population from Russia. Ten SNPs (rs310216, rs3212780, rs12693591, rs2293152, rs28362491, rs4711998, rs1974226, rs1501299, rs266729, and rs12733285) were genotyped by the real-time polymerase chain reaction (TaqMan assays) in a case–control study (425 COPD patients and 457 in the control group, from Ufa, Russia). Logistic regression was used to detect the association of SNPs in different models. Linear regression analyses were performed to estimate the relationship between SNPs and lung function parameters and pack-years. In Tatar population, significant associations of JAK1 (rs310216) (P = 0.0002, OR 1.70 in additive model), JAK3 (rs3212780) (P = 0.001, OR 1.61 in dominant model), and IL17A (rs1974226) (P = 0.0037, OR 2.31 in recessive model) with COPD were revealed. The disease risk was higher in carriers of insertion allele of NFKB1 (rs28362491) (P = 0.045, OR 1.22). We found a significant gene-by-environment interaction of smoking status and IL17A (rs1974226) (P interact = 0.016), JAK3 (rs3212780) (P interact = 0.031), ADIPOQ (rs266729) (P interact = 0.013), and ADIPOR1 (rs12733285) (P interact = 0.018). The relationship between the rs4711998, rs1974226, rs310216, rs3212780, rs28362491, and smoking pack-years was found (P = 0.045, P = 0.004, P = 0.0005, P = 0.021, and P = 0.042). A significant genotype-dependent variation of forced vital capacity was observed for NFKB1 (rs28362491) (P = 0.017), ADIPOR1 (rs12733285) (P = 0.043), and STAT1 (rs12693591) (P = 0.048). The genotypes of STAT1 (rs12693591) (P = 0.013) and JAK1 (rs310216) (P = 0.048) were associated with forced expiratory volume in 1 s.

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References

  1. Bianco A, Mazzarella G, Turchiarelli V, Nigro E, Corbi G, Scudiero O, Sofia M, Daniele A (2013) Adiponectin: an attractive marker for metabolic disorders in chronic obstructive pulmonary disease (COPD). Nutrients 5(10):4115–4125. doi:10.3390/nu5104115

    Article  PubMed  PubMed Central  Google Scholar 

  2. Caporaso N, Gu F, Chatterjee N, Sheng-Chih J, Yu K, Yeager M, Chen C, Jacobs K, Wheeler W, Landi MT, Ziegler RG, Hunter DJ, Chanock S, Hankinson S, Kraft P, Bergen AW (2009) Genome-wide and candidate gene association study of cigarette smoking behaviors. PLoS One 4(2):e4653. doi:10.1371/journal.pone.0004653

    Article  PubMed  PubMed Central  Google Scholar 

  3. Carolan BJ, Hughes G, Morrow J, Hersh CP, O’Neal WK, Rennard S, Pillai SG, Belloni P, Cockayne DA, Comellas AP, Han M, Zemans RL, Kechris K, Bowler RP (2014) The association of plasma biomarkers with computed tomography-assessed emphysema phenotypes. Respir Res 15:127. doi:10.1186/s12931-014-0127-9

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chang Y, Al-Alwan L, Audusseau S, Chouiali F, Carlevaro-Fita J, Iwakura Y, Baglole CJ, Eidelman DH, Hamid Q (2014) Genetic deletion of IL-17A reduces cigarette smoke-induced inflammation and alveolar type II cell apoptosis. Am J Physiol Lung Cell Mol Physiol 306(2):L132–L143. doi:10.1152/ajplung.00111.2013

    CAS  Article  PubMed  Google Scholar 

  5. Chen JM, Ferec C, Cooper DN (2006) A systematic analysis of disease-associated variants in the 3′ regulatory regions of human protein-coding genes I: general principles and overview. Hum Genet 120:1–21. doi:10.1007/s00439-006-0180-7

    CAS  Article  PubMed  Google Scholar 

  6. Cho MH, Boutaoui N, Klanderman BJ, Sylvia JS, Ziniti JP, Hersh CP et al (2010) Variants in FAM13A are associated with chronic obstructive pulmonary disease. Nat Genet 42:200–202. doi:10.1038/ng.535

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Dariusz B, Agnieszka SM, Daniel K, Anna B, Adam KS (2014) Polymorphism of interleukin-17 and its relation to mineral density of bones in perimenopausal women. Eur J Med Res 19(1):69. doi:10.1186/s40001-014-0069-1

    Article  Google Scholar 

  8. de Faria AP, Modolo R, Sabbatini AR, Barbaro NR, Corrêa NB, Brunelli V, Tanus-Santos JE, Fontana V, Moreno H (2015) Adiponectin −11377C/G and +276G/T polymorphisms affect adiponectin levels but do not modify responsiveness to therapy in resistant hypertension. Basic Clin Pharmacol Toxicol 117(1):65–72. doi:10.1111/bcpt.12368

    Article  PubMed  Google Scholar 

  9. Di Stefano A, Caramori G, Gnemmi I, Contoli M, Vicari C, Capelli A, Magno F, D’Anna SE, Zanini A, Brun P, Casolari P, Chung KF, Barnes PJ, Papi A, Adcock I, Balbi B (2009) T helper type 17-related cytokine expression is increased in the bronchial mucosa of stable chronic obstructive pulmonary disease patients. Clin Exp Immunol 157(2):316–324. doi:10.1111/j.1365-2249.2009.03965.x

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ding Y, Niu H, Zhou L, Zhou W, Chen J, Xie S, Geng T, Ouyang Y, He P, Sun P, Feng T, Jin T (2015a) Association of multiple genetic variants with chronic obstructive pulmonary disease (COPD) susceptibility in Hainan region. Clin Respir J. doi:10.1111/crj.12407

    Google Scholar 

  11. Ding Y, Yang D, Zhou L, Xu J, Chen Y, He P, Yao J, Chen J, Niu H, Sun P, Jin T (2015b) Variants in multiple genes polymorphism association analysis of COPD in the Chinese Li population. Int J Chron Obstr Pulmon Dis 10:1455–1463. doi:10.2147/COPD.S86721

    Article  Google Scholar 

  12. Eustace A, Smyth LJ, Mitchell L, Williamson K, Plumb J, Singh D (2011) Identification of cells expressing IL-17A and IL-17 F in the lungs of patients with COPD. Chest 139:1089–1100

    Article  PubMed  Google Scholar 

  13. Fantuzzi G (2013) Adiponectin in inflammatory and immune-mediated diseases. Cytokine 64(1):1–10

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Farahani R, Sherkat R, Hakemi MG, Eskandari N, Yazdani R (2014) Cytokines (interleukin-9, IL-17, IL-22, IL-25 and IL-33) and asthma. Adv Biomed Res 3:127. doi:10.4103/2277-9175.133249

    Article  PubMed  PubMed Central  Google Scholar 

  15. Franssen FM, O’Donnell DE, Goossens GH, Blaak EE, Schols AM (2008) Obesity and the lung: 5. obesity and COPD. Thorax 63(12):1110–1117

    CAS  Article  PubMed  Google Scholar 

  16. Geraghty P, Wyman AE, Garcia-Arcos I, Dabo AJ, Gadhvi S, Foronjy R (2013) STAT3 modulates cigarette smoke-induced inflammation and protease expression. Front Physiol 4:267. doi:10.3389/fphys.2013.00267

    Article  PubMed  PubMed Central  Google Scholar 

  17. Global Strategy for the Diagnosis, Management and Prevention of Chronic Obstructive Pulmonary Disease, Global Initiative for Chronic Obstructive Lung Disease (GOLD) (Updated 2011). http://www.goldcopd.org/

  18. Hackett TL, Holloway R, Holgate ST, Warner JA (2008) Dynamics of pro-inflammatory and anti-inflammatory cytokine release during acute inflammation in chronic obstructive pulmonary disease: an ex vivo study. Respir Res 29(9):47. doi:10.1186/1465-9921-9-47

    Article  Google Scholar 

  19. Heid IM, Henneman P, Hicks A, Coassin S, Winkler T, Aulchenko YS et al (2010) Clear detection of ADIPOQ locus as the major gene for plasma adiponectin: results of genome-wide association analyses including 4659 European individuals. Atherosclerosis 208(2):412–420

    CAS  Article  PubMed  Google Scholar 

  20. Hou S, Qi J, Zhang Q, Liao D, Li Q, Hu K, Zhou Y, Kijlstra A, Yang P (2013) Genetic variants in the JAK1 gene confer higher risk of Behcet’s disease with ocular involvement in Han Chinese. Hum Genet 132(9):1049–1058

    CAS  Article  PubMed  Google Scholar 

  21. Hsieh YY, Chang CC, Hsu CM, Wan L, Chen SY, Lin WH, Tsai FJ (2011) JAK-1 rs2780895 C-related genotype and allele but not JAK-1 rs10789166, rs4916008, rs2780885, rs17127114, and rs3806277 are associated with higher susceptibility to asthma. Genet Test Mol Biomark 15:841–847

    CAS  Article  Google Scholar 

  22. Hu K, Hou S, Li F, Xiang Q, Kijlstra A, Yang P (2013) JAK1, but not JAK2 and STAT3, confers susceptibility to Vogt-Koyanagi-Harada (VKH) syndrome in Han Chinese population. Invest Ophthalmol Vis Sci 54(5):3360–3365

    CAS  Article  PubMed  Google Scholar 

  23. International Statistical Classification of Diseases and Related Health Problems, Tenth Revision (2015) (ICD-10 http://www.who.int/classifications/icd/en/)

  24. Jiang B, Zhu ZZ, Liu F, Yang LJ, Zhang WY, Yuan HH, Wang JG, Hu XH, Huang G (2011) STAT3 gene polymorphisms and susceptibility to non-small cell lung cancer. Genet Mol Res 10(3):1856–1865. doi:10.4238/vol10-3gmr1071

    CAS  Article  PubMed  Google Scholar 

  25. Jin Y, Deng Z, Cao C, Li L (2015) IL-17 polymorphisms and asthma risk: a meta-analysis of 11 single nucleotide polymorphisms. J Asthma 52(10):981–988. doi:10.3109/02770903.2015

    CAS  Article  PubMed  Google Scholar 

  26. Karban AS, Okazaki T, Panhuysen CI, Gallegos T, Potter JJ, Bailey-Wilson JE et al (2004) Functional annotation of a novel NFKB1promoter polymorphism that increases risk for ulcerative colitis. Hum Mol Genet 13:35–45

    CAS  Article  PubMed  Google Scholar 

  27. Korn T, Bettelli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 Cells. Ann Rev Immunol 27:485–517

    CAS  Article  Google Scholar 

  28. Kurimoto E, Miyahara N, Kanehiro A, Waseda K, Taniguchi A, Ikeda G, Koga H, Nishimori H, Tanimoto Y, Kataoka M, Iwakura Y, Gelfand EW, Tanimoto M (2013) IL-17A is essential to the development of elastase-induced pulmonary inflammation and emphysema in mice. Respir Res 14:5. doi:10.1186/1465-9921-14-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Kuruma S, Egawa N, Kurata M, Honda G, Kamisawa T, Ueda J, Ishii H, Ueno M, Nakao H et al (2014) Case-control study of diabetes-related genetic variants and pancreatic cancer risk in Japan. World J Gastroenterol 20(46):17456–17462

    Article  PubMed  PubMed Central  Google Scholar 

  30. Lai H-M, Li X-M, Yang Y-N, Ma Y-T, Xu R, Pan S et al (2015) Genetic variation in NFKB1 and NFKBIA and susceptibility to coronary artery disease in a chinese uygur population. PLoS One 10(6):e0129144. doi:10.1371/journal.pone.0129144

    Article  PubMed  PubMed Central  Google Scholar 

  31. Laumen H, Saningong AD, Heid IM, Hess J, Herder C, Claussnitzer M et al (2009) Functional characterization of promoter variants of the adiponectin gene complemented by epidemiological data. Diabetes 58:9849–9891. doi:10.2337/db07-1646

    Article  Google Scholar 

  32. Lawrence T (2009) The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 1(6):a001651. doi:10.1101/cshperspect.a001651

    Article  PubMed  PubMed Central  Google Scholar 

  33. Leu HB, Chung CM, Lin SJ, Jong YS, Pan WH, Chen JW (2011) Adiponectin gene polymorphism is selectively associated with the concomitant presence of metabolic syndrome and essential hypertension. PLoS One 6:e19999. doi:10.1371/journal.pone.0019999

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Lill CM, Schjeide BM, Akkad DA, Blaschke P, Winkelmann A, Gerdes LA, Hoffjan S, Luessi F, Dörner T, Li SC et al (2012) Independent replication of STAT3 association with multiple sclerosis risk in a large German case-control sample. Neurogenetics 13(1):83–86

    CAS  Article  PubMed  Google Scholar 

  35. López-Mejías R, García-Bermúdez M, González-Juanatey C, Castañeda S, Miranda-Filloy JA, Gómez-Vaquero C, Fernández-Gutiérrez B, Balsa A, Pascual-Salcedo D, Blanco R, González-Álvaro I, Llorca J, Martín J, González-Gay MA (2012) NFKB1-94ATTG ins/del polymorphism (rs28362491) is associated with cardiovascular disease in patients with rheumatoid arthritis. Atherosclerosis 224(2):426–429

    Article  PubMed  Google Scholar 

  36. Mathew CG (1985) The isolation of high molecular weight eukaryotic DNA. Methods Mol Biol 2:31–34

    CAS  PubMed  Google Scholar 

  37. McGovern DP, Rotter JI, Mei L, Haritunians T, Landers C, Derkowski C, Dutridge D, Dubinsky M, Ippoliti A, Vasiliauskas E, Mengesha E, King L, Pressman S, Targan SR, Taylor KD (2009) Genetic epistasis of IL23/IL17 pathway genes in Crohn’s disease. Inflamm Bowel Dis 15(6):883–889

    Article  PubMed  PubMed Central  Google Scholar 

  38. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A et al (2005) Standardisation of spirometry. Eur Respir J 26:319–338

    CAS  Article  PubMed  Google Scholar 

  39. Miller M, Cho JY, Pham A, Ramsdell J, Broide DH (2009) Adiponectin and functional adiponectin receptor 1 are expressed by airway epithelial cells in chronic obstructive pulmonary disease. J Immunol 182:684–691

    CAS  Article  PubMed  Google Scholar 

  40. Nakada TA, Russell JA, Boyd JH, Walley KR (2011) IL17A genetic variation is associated with altered susceptibility to Gram-positive infection and mortality of severe sepsis. Crit Care 15(5):R254. doi:10.1186/cc10515

    Article  PubMed  PubMed Central  Google Scholar 

  41. Open database of single nucleotide polymorphisms (SNPs) and multiple small-scale variations that include insertions/deletions, microsatellites, and non-polymorphic variants. Bethesda (MD): The National Center for Biotechnology Information advances science and health by providing access to biomedical and genomic information (US). http://www.ncbi.nlm.nih.gov/projects/SNP/

  42. Pallavi S, Anoop K, Showket H, Alo N, Mausumi B (2015) NFKB1/NFKBIa polymorphisms are associated with the progression of cervical carcinoma in HPV-infected postmenopausal women from rural area. Tumour Biol 36(8):6265–6276

    CAS  Article  PubMed  Google Scholar 

  43. Pillai SG, Ge D, Zhu G, Kong X, Shianna KV, Need AC et al (2009) A genome-wide association study in chronic obstructive pulmonary disease (COPD): identification of two major susceptibility loci. PLoS Genet 5:e1000421. doi:10.1371/journal.pgen.1000421

    Article  PubMed  PubMed Central  Google Scholar 

  44. Pillai SG, Kong X, Edwards LD, Cho MH, Anderson WH, Coxson HO et al (2010) Loci identified by genome-wide association studies influence different disease-related phenotypes in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 182:1498–1505. doi:10.1164/rccm.201002-0151OC

    Article  PubMed  PubMed Central  Google Scholar 

  45. Pinto LA, Steudemann L, Depner M, Klopp N, Illig T, Weiland SK, von Mutius E, Kabesch M (2007) STAT1 gene variations, IgE regulation and atopy. Allergy 62(12):1456–1461

    CAS  Article  PubMed  Google Scholar 

  46. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC (2007) PLINK: a toolset for whole-genome association and population-based linkage analysis. Am J Hum Genet 81:559–575

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC (1993) Lung volumes and forced ventilatory flows. Report working party standardization of lung function tests, European community for steel and coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl 16:5–40

    CAS  Article  PubMed  Google Scholar 

  48. Rafiei A, Hosseini V, Janbabai G, Ghorbani A, Ajami A, Farzmandfar T, Azizi MD, Gilbreath JJ, Merrell DS (2013) Polymorphism in the interleukin-17A promoter contributes to gastric cancer. World J Gastroenterol 19(34):5693–5699

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  49. Ramana CV, Chatterjee-Kishore M, Nguyen H, Stark GR (2000) Complex roles of Stat1 in regulating gene expression. Oncogene 19(21):2619–2627

    CAS  Article  PubMed  Google Scholar 

  50. Rasouli M, Asaei S, Kalani M, Kiany S, Moravej A (2013) Interleukin-17A genetic variants can confer resistance to brucellosis in Iranian population. Cytokine 61(1):297–303

    CAS  Article  PubMed  Google Scholar 

  51. Rawlings JS, Rosler KM, Harrison DA (2004) The JAK/STAT signaling pathway. J Cell Sci 117(Pt 8):1281–1283

    CAS  Article  PubMed  Google Scholar 

  52. Roca J, Burgos F, Barberà JA, Sunyer J, Rodriguez-Roisin R, Castellsagué J et al (1998) Prediction equations for plethysmographic lung volumes. Respir Med 92:454–460

    CAS  Article  PubMed  Google Scholar 

  53. Roos AB, Sandén C, Mori M, Bjermer L, Stampfli MR, Erjefält JS (2015) IL-17A is elevated in end-stage COPD and contributes to cigarette smoke-induced lymphoid neogenesis. Am J Respir Crit Care Med 191(11):1232–1241

    CAS  Article  PubMed  Google Scholar 

  54. Sato K, Shibata Y, Abe S, Inoue S, Igarashi A, Yamauchi K, Aida Y, Nunomiya K et al (2014) Association between plasma adiponectin levels and decline in forced expiratory volume in 1 s in a general Japanese population: the Takahata study. Int J Med Sci 11(8):758–764

    Article  PubMed  PubMed Central  Google Scholar 

  55. Siedlinski M, Cho MH, Bakke P, Gulsvik A, Lomas DA, Anderson W et al (2011) Genome-wide association study of smoking behaviours in patients with COPD. Thorax 66:894–902. doi:10.1136/thoraxjnl-2011-200154

    Article  PubMed  PubMed Central  Google Scholar 

  56. Solé X, Guinó E, Valls J, Iniesta R, Moreno V (2006) SNPStats: a web tool for the analysis of association studies. Bioinformatics 22:1928–1929

    Article  PubMed  Google Scholar 

  57. Sperati CJ, Parekh RS, Berthier-Schaad Y, Jaar BG, Plantinga L, Fink N, Powe NR, Smith MW, Coresh J, Kao WH (2009) Association of single-nucleotide polymorphisms in JAK3, STAT4, and STAT6 with new cardiovascular events in incident dialysis patients. Am J Kidney Dis 53(5):845–855

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Vasseur F, Helbecque N, Dina C, Lobbens S, Delannoy V, Gaget S et al (2002) Single-nucleotide polymorphism haplotypes in the both proximal promoter and exon 3 of the APM1 gene modulate adipocyte-secreted adiponectin hormone levels and contribute to the genetic risk for type 2 diabetes in French Caucasians. Hum Mol Genet 11:2607–2614

    CAS  Article  PubMed  Google Scholar 

  59. Wang K, Zhou B, Zhang J, Xin Y, Lai T, Wang Y, Hou Q, Song Y, Chen Y, Quan Y, Xi M, Zhang L (2011) Association of signal transducer and activator of transcription 3 gene polymorphisms with cervical cancer in Chinese women. DNA Cell Biol 30(11):931–936. doi:10.1089/dna.2010.1179

    CAS  Article  PubMed  Google Scholar 

  60. Wang Z, Liu QL, Sun W, Yang CJ, Tang L, Zhang X, Zhong XM (2014a) Genetic polymorphisms in inflammatory response genes and their associations with breast cancer risk. Croat Med J 55(6):638–646

    Article  PubMed  PubMed Central  Google Scholar 

  61. Wang Z, Xu B, Zhang H, Fan R, Zhou J, Zhong J (2014b) Association between STAT3 gene polymorphisms and Crohn’s disease susceptibility: a case-control study in a Chinese Han population. Diagn Pathol 9:104. doi:10.1186/1746-1596-9-104

    Article  PubMed  PubMed Central  Google Scholar 

  62. Wang Q, Zhu XC, Liu H, Ran MS, Fang DZ (2015a) A longitudinal study of the association of adiponectin gene rs1501299 with depression in Chinese Han adolescents after Wenchuan earthquake. J Affect Disord 175:86–91. doi:10.1016/j.jad.2014.12.056

    CAS  Article  PubMed  Google Scholar 

  63. Wang X, Peng H, Liang Y, Sun R, Wei T, Li Z, Gong Y, Gong R, Liu F, Zhang L, Zhu JA (2015b) functional insertion/deletion polymorphism in the promoter region of the NFKB1 gene increases the risk of papillary thyroid carcinoma. Genet Test Mol Biomark 19(3):167–171

    CAS  Article  Google Scholar 

  64. Woo JG, Dolan LM, Deka R, Kaushal RD, Shen Y, Pal P, Daniels SR, Martin LJ (2006) Interactions between noncontiguous haplotypes in the adiponectin gene ACDC are associated with plasma adiponectin. Diabetes 55:523–529

    CAS  Article  PubMed  Google Scholar 

  65. Xiao L, Muhali FS, Cai TT, Song RH, Hu R, Shi XH, Jiang WJ, Li DF, He ST, Xu J, Zhang JA (2013) Association of single-nucleotide polymorphisms in the STAT3 gene with autoimmune thyroid disease in Chinese individuals. Funct Integr Genomics 13(4):455–461

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. Xie HJ, Bae HJ, Noh JH, Eun JW, Kim JK, Jung KH, Ryu JC et al (2009) Mutational analysis of JAK1 gene in human hepatocellular carcinoma. Neoplasma 56:136–140

    CAS  Article  PubMed  Google Scholar 

  67. Yang Y, Zhang F, Ding R, Wang Y, Lei H, Hu D (2012) Association of ADIPOQ gene polymorphisms and coronary artery disease risk: a meta-analysis based on 12 465 subjects. Thromb Res 130:58–64. doi:10.1016/j.thromres.2012.01.018

    CAS  Article  PubMed  Google Scholar 

  68. Yang YN, Zhang JY, Ma YT, Xie X, Li XM, Liu F, Chen BD, Dong XH, Zheng YY, Pan S, Zhai H, Li DZ, Chen QJ (2014) 94 ATTG insertion/deletion polymorphism of the NFKB1 gene is associated with coronary artery disease in Han and Uygur women in China. Genet Test Mol Biomark 18(6):430–438

    CAS  Article  Google Scholar 

  69. Yuan Y, Jiang H, Kuang J, Hou X, Feng Y, Su Z (2012) Genetic variations in ADIPOQ gene are associated with chronic obstructive pulmonary disease. PLoS One 7(11):e50848. doi:10.1371/journal.pone.0050848

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  70. Yuan K, Liu H, Huang L, Ren X, Liu J, Dong X, Tian W, Jia Y (2014) rs744166 polymorphism of the STAT3 gene is associated with risk of gastric cancer in a Chinese population. Biomed Res Int. doi:10.1155/2014/527918

    Google Scholar 

  71. Zhang D, Ma J, Brismar K, Efendic S, Gu HF (2009) A single nucleotide polymorphism alters the sequence of SP1 binding site in the adiponectin promoter region and is associated with diabetic nephropathy among type 1 diabetic patients in the genetics of kidneys in diabetes study. J Diabetes Complicat 23:265–272. doi:10.1016/j.jdiacomp.2008.05.004

    Article  PubMed  Google Scholar 

  72. Zhang D, Li L, Zhu Y, Zhao L, Wan L, Lv J, Li X, Huang P, Wei L, Ma M (2013) The NFKB1-94 ATTG insertion/deletion polymorphism (rs28362491) contributes to the susceptibility of congenital heart disease in a Chinese population. Gene 516(2):307–310

    CAS  Article  PubMed  Google Scholar 

  73. Zhong Y, Wu J, Chen B, Ma R, Cao H, Wang Z, Cheng L, Ding J, Feng J (2012) Investigation and analysis of single nucleotide polymorphisms in Janus kinase/signal transducer and activator of transcription genes with leukemia. Leuk Lymph 53(6):1216–1221. doi:10.3109/10428194.2011.645212

    CAS  Article  Google Scholar 

  74. Zhou B, Rao L, Peng Y, Wang Y, Li Y, Gao L, Chen Y, Xue H, Song Y, Liao M, Zhang L (2009) Functional polymorphism of the NFKB1 gene promoter is related to the risk of dilated cardiomyopathy. BMC Med Genet 10:47. doi:10.1186/1471-2350-10-47

    Article  PubMed  PubMed Central  Google Scholar 

  75. Zhu ZZ, Di JZ, Gu WY, Cong WM, Gawron A, Wang Y, Zheng Q, Wang AZ, Zhu G, Zhang P, Hou L (2010) Association of genetic polymorphisms in STAT1 gene with increased risk of hepatocellular carcinoma. Oncology 78(5–6):382–388

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Russian Foundation for Basic Research Grants (Nos. 13-04-00287, 14-04-97006, and 14-06-97003), and the Russian Foundation for Humanities Grant No. 16-06-00162).

Author Contributions

The conception and study design of the work: G. F. Korytina, T.V. Viktorova, Sh.Z. Zagidullin. The patients and control—medical examination and selection: Y.G. Aznabaeva, Sh.Z. Zagidullin. Performing the experiment (case and control—DNA-collecting; real-time PCR): G. F. Korytina, L. Z. Akhmadishina, O.V. Kochetova. Genetic association analysis: G. F. Korytina, L. Z. Akhmadishina, O.V. Kochetova. Statistical analysis: G. F. Korytina. Interpretation of data for the work: G. F. Korytina, T.V. Viktorova, Z. Akhmadishina, O.V. Kochetova, Y.G. Aznabaeva, Sh.Z. Zagidullin. Manuscript writing: G. F. Korytina, T.V. Viktorova, L. Z. Akhmadishina, Y.G. Aznabaeva, Sh.Z. Zagidullin, O.V. Kochetova. Review of the manuscript: G. F. Korytina, T.V. Viktorova, L. Z. Akhmadishina, Y.G. Aznabaeva, Sh.Z. Zagidullin., O.V. Kochetova.

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  1. Department of Genomics, Institute of Biochemistry and Genetics, Russian Academy of Sciences, Pr. Oktybry, 71, Ufa, Russian Federation, 450054

    Gulnaz Faritovna Korytina, L. Z. Akhmadishina, O. V. Kochetova & T. V. Victorova

  2. Department of Biology and Department of Internal Diseases, Bashkortostan State Medical University, Lenina st., 3, Ufa, Russian Federation, 450000

    Y. G. Aznabaeva, Sh. Z. Zagidullin & T. V. Victorova

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  1. Gulnaz Faritovna Korytina
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Correspondence to Gulnaz Faritovna Korytina.

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Korytina, G.F., Akhmadishina, L.Z., Kochetova, O.V. et al. Inflammatory and Immune Response Genes Polymorphisms are Associated with Susceptibility to Chronic Obstructive Pulmonary Disease in Tatars Population from Russia. Biochem Genet 54, 388–412 (2016). https://doi.org/10.1007/s10528-016-9726-0

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Keywords

  • Chronic obstructive pulmonary disease
  • Association
  • Chronic inflammation
  • Cytokines
  • JAK/STAT-signaling
  • Adiponectin