STAT6 - Polymorphisms, haplotypes and epistasis in relation to atopy and asthma

Biomedical Papers

Volumn 157, Issue 2, 2013, Pages 172-180

  Godava, Marek ^a,b   Vrtel, Radek ^a,b   Vodicka, Radek ^a,b  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b UNIVERSITY HOSPITAL OLOMOUC   (Czech Republic)

Author keywords

Asthma; Atopy; Epistasis; Haplotypes; IgE; Polymorphisms; STAT6

Indexed keywords

IMMUNOGLOBULIN E; STAT6 PROTEIN; STAT6 PROTEIN, HUMAN;

ARTICLE; ASTHMA; EPISTASIS; GENETIC PREDISPOSITION; GENETICS; HAPLOTYPE; HUMAN; METABOLISM; SINGLE NUCLEOTIDE POLYMORPHISM;

ASTHMA; EPISTASIS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; IMMUNOGLOBULIN E; POLYMORPHISM, SINGLE NUCLEOTIDE; STAT6 TRANSCRIPTION FACTOR;

EID: 84879346003     PISSN: 12138118     EISSN: 18047521     Source Type: Journal    
DOI: 10.5507/bp.2013.043     Document Type: Article

References (74)

1. Jarvis D, Burney P. The epidemiology of allergic disease. BMJ 1998;316(7131):607-10.
2. Shapira SK, Vercelli D, Jabara HH, Fu SM, Geha RS. Molecular analysis of the induction of immunoglobulin E synthesis in human B cells by interleukin 4 and engagement of CD40 antigen. J Exp Med 1992;175(1):289-92.
3. Magnusson CG. Cord serum IgE in relation to family history and as predictor of atopic disease in early infancy. Allergy 1988;43:241-51.
4. Liu CA, Wang CL, Chuang H, Ou CY, Hsu TY, Yang KD. Prenatal prediction of infant atopy by maternal but not paternal total IgE levels. J Allergy Clin Immunol 2003;112:899-904.
5. Yang KD, Ou CY, Hsu TY, Chang JC, Chuang H, Liu CA, Liang HM., Kuo HC, Chen RF, Huang EY. Interaction of maternal atopy, CTLA-4 gene polymorphism and gender on antenatal immunoglobulin E production. Clinical and Experimental Allergy 2007;37:680-7.
6. Canfield SM, Jacobson JS, Perzanowski MS, Mellins RB, Zemble RM, Cheb GL, Goldstein IF. Total and specific IgE associations between New York City Head Start children and their parents. J Allergy Clin Immunol 2008;121:1422-7.
7. Cookson WO, Young RP, Sandford AJ, Moffatt MF, Shirakawa T, Sharp PA, Faux JA, Julier C, Nakumuura Y. Maternal inheritance of atopic IgE responsiveness on chromosome 11q. Lancet 1992;340:381-4.
8. Raby BA, Soto-Quiros ME, Avila L Lake SL, Murény A, Liang C, Fournier E, Spesny M, Sylvia JS, Verner A, Hudson TJ, Klanderman BJ, Freimer NB, Silverman EK, Celedón JC. Sex-specific linkage to total serum immunoglobulin E in families of children with asthma in Costa Rica. Human Molecular Genetics 2007;16:243-53.
9. Weidinger S, Gieger C, Rodriguez E, Baurecht H, Mempel M, Klopp N, Gohlke H, Wagenpfeil S, Ollert M, Ring J, Behrendt H, Heinrich J, Novak N, Bieber T, Krämer U, Berdel D, von Berg A, Bauer CP, Herbarth O, Koletzko S, Prokisch H, Mehta D, Meitinger T, Depner M, von Mutius E, Liang L, Moffatt M, Cookson W, Kabesch M, Wichmann HE, Illig T. Genome-Wide Scan on Total Serum IgE Levels Identifies FCER1A as Novel Susceptibility Locus. PLoS Genet 2008;4(8):e1000166. doi: 10.1371/journal.pgen.100016
10. Marsh DG, Neely JD, Breazeale DR, Ghosh B, Freidhoff LR, Ehrlich-Kautzky E, Schou C, Krishnaswamy G, Beaty TH. Linkage analysis of IL-4 and other chromosome 5q31.1 markers and total serum immunoglobulin E concentrations. Science 1994;264(5162):1152-6.
11. The collaborative study on the genetics of asthma. A genome-wide search for asthma susceptibility loci in ethnically diverse populations. Nat Genet 1997;15:389-92.
12. Deichmann KA, Heinzmann A, Forster J, Dischinger S, Mehl C, Brueggenolte E, Hildebrandt F, Moseler M, Kuehr J. Linkage and allelic association of atopy and markers flanking the IL-4-receptor gene. Clin Exp Allergy 1997;28(2):151-5.
13. Kabesch M., Schedel M, Carr D, Woitsch B, Fritzsch Ch, Stephan K, Weiland SK, Murous E. IL-4/IL-13 pathway genetics strongly influence serum IgE levels and childhood asthma. J Allergy Clin Immunol 2006;117:269-74.
14. Barnes KC, Neely JD, Duffy DL, Freidhoff LR, Breazeale DR, Schou C, Naidu RP, Levett PN, Renault B, Kucherlapati R, Iozzino S, Ehrlich E, Beaty TH, Marsh DG. Linkage of asthma and total serum IgE concentration to markers on chromosome 12q: evidence from Afro-Caribbean and Caucasian populations. Genomics 1996;37:41-50.
15. Nickel R, Wahn U, Hizawa N, Maestri N, Duffy DL, Barnes KC, Beyer K, Forster J, Bergmann R, Zepp F, Wahn V, Marsh DG. Evidence for linkage of chromosome 12q15-q24.1 markers to high total serum IgE concentrations in children of the German Multicenter Allergy Study. Genomics 1997;46:159-62.
16. Barnes KC, Freidhoff LR, Nickel R, Chiu YF, Juo SH, Hizawa N, Naidu RP, Ehrlich E, Duffy DL, Schou C, Levett PN, Marsh DG, Beaty TH.: Densemapping of chromosome 12q13.12-q23.3 and linkage to asthma and atopy. J Allergy Clin Immunol 1999;104:485-91.
17. Hou J, Schindler U, Henzel WJ, Ho TC, Brasseur M, McKnight SL. An interleukin-4-induced transcription factor: IL-4 stat. Science 1994;265:1701-6.
18. Quelle FW, Shimoda K, Thierfelder W, Fischer C, Kim A, Ruben SM, Cleveland JL, Pierce JH, Keegan AD, Nelms K, Paul WE, Ihle JN. Cloning of murine Stat6 and human Stat6, Stat proteins that are tyrosine phosphorylated in responses to Il-4 and Il-3 but are not required for mitogenesis. Molecular and cellular biology 1995;15:3336-43.
19. Patel BK, Keck CL, O'Leary RS, Popescu NC, LaRochelle WJ. Localization of the human stat6 gene to chromosome 12q13.3- q14.1, a region implicated in multiple solid tumors. Genomics 1998;52:192-200.
20. Patel BK, Wang LM, Lee CC, Taylor WG, Pierce JH, La Rochelle WJ. Stat6 and Jak1 are common elements in platelet-derived growth factor and interleukin-4 signal transduction pathways in NIH 3T3 fibroblasts. J Biol Chem 1996;271:22175-82.
21. Patel BK, Pierce JH, LaRochelle WJ. Regulation of interleukin 4-mediated signaling by naturally occurring dominant negative and attenuated forms of human Stat6. Proc Natl Acad Sci U S A 1998;95:172-7.
22. Hebenstreit D, Wirnsberger G, Horejs-Hoeck J, Duschl A. Signaling mechanisms, interaction partners, and target genes of STAT6. Cytokine Growth Factor Rev 2006;17(3):173-88.
23. Schedel M, Frei R, Bieli Ch, Cameron L, Adamski J, Lauener R and Kabesch M. An IgE-associated polymorphism in STAT6 alters NF-kB binding, STAT6 promoter activity, and mRNA expression. J Allergy Clin Immunol 2009;124(3):583-9.
24. Wurster AL, Tanaka T, Grusby MJ. The biology of Stat4 and Stat6. Oncogene 2000;19(21):2577-84.
25. Xu X, Sun YL, Hoey T. Cooperative DNA binding and sequence-selective recognition conferred by the STAT amino-terminal domain. Science 1996;273(5276):794-7.
26. Vinkemeier U, Cohen SL, Moarefi I, Chait BT, Kuriyan J, Darnell JE Jr. DNA binding of in vitro activated Stat1 alpha, Stat1 beta and truncated Stat1: interaction between NH2-terminal domains stabilizes binding of two dimers to tandem DNA sites. EMBO J 1996;15(20):5616-26.
27. Musacchio A, Gibson T, Lehto VP, Saraste M. SH3, an abundant protein domain in search of a function. FEBS Lett 1992;307:55-61.
28. Morton CJ, Campbell ID. SH3 domains. Molecular 'Velcro'. Curr Biol 1994;4:615-7.
29. Pawson T, Gish GD. SH2 and SH3 domains: from structure to function. Cell 1992;71:359-62.
30. Mikita T, Daniel C, Wu P, Schindler U. Mutational analysis of the STAT6 SH2 domain. J Biol Chem 1998;273(28):17634-42.
31. Litterst CM, Pfitzner E. Transcriptional activation by STAT6 requires the direct interaction with NCoA-1. J Biol Chem 2001;276(49):45713-21.
32. Delphin S, Stavnezer J. Characterization of an interleukin 4 (IL-4) responsive region in the immunoglobulin heavy chain germline epsilon promoter: regulation by NF-IL-4, a C/EBP family member and NF-kappa B/p50. J Exp Med 1995;181(1):181-92.
33. Shimoda K, van Deursen J, Sangster MY, Sarawar SR, Carson RT, Tripp RA, Chu C, Quelle FW, Nosaka T, Vignali DA, Doherty PC, Grosveld G, Paul WE, Ihle JN. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 1996;380(6575):630-3.
34. Kaplan MH, Schindler U, Smiley ST, Grusby MJ. Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 1996;4(3):313-9.
35. Mikita T, Campbell D, Wu P, Williamson K, Schindler U. Requirements for interleukin-4-induced gene expression and functional characterization of Stat6. Mol Cell Biol 1996;16(10):5811-20.
36. Leonard WJ, O'Shea JJ. Jaks and STATs: Biological implications. Annu Rev Immunol 1998;16:293-322.
37. Chatila TA. Interleukin-4 receptor signaling pathways in asthma pathogenesis. Trends Mol Med 2004;10(10):493-9.
38. Wjst M, Fischer G, Immervoll T, Jung M, Saar K, Rueschendorf F, Reis A, Ulbrecht M, Gomolka M, Weiss EH, Jaeger L, Nickel R, Richter K, Kjellman NI, Griese M, von Berg A, Gappa M, Riedel F, Boehle M, van Koningsbruggen S, Schoberth P, Szczepanski R, Dorsch W, Silbermann M, Wichmann HE. A genome-wide search for linkage to asthma. German Asthma Genetics Group. Genomics 1999;15;58(1): 1-8.
39. Tamura K, Arakawa H, Suzuki M, Kobayashi Y, Mochizuki H, Kato M, Tokuyama K, Morikawa A. Novel dinucleotide repeat polymorphism in the first exon of the STAT-6 gene is associated with allergic diseases. Clin Exp Allergy 2001;31(10):1509-14.
40. Duetsch G, Illig T, Loesgen S, Rohde K, Klopp N, Herbon N, Gohlke H, Altmueller J, Wjst M. STAT6 as an asthma candidate gene: polymorphism-screening, association and haplotype analysis in a Caucasian sib-pair study. Hum Mol Genet 2002;11(6):613-21.
41. Gao PS, Heller NM, Walker W, Chen CH, Moller M, Plunkett B, Roberts MH, Schleimer RP, Hopkin JM, Huang SK. Variation in dinucleotide (GT) repeat sequence in the first exon of the STAT6 gene is associated with atopic asthma and differentially regulates the promoter activity in vitro. J Med Genet 2004;41(7):535-9.
42. Nagarkatti R, B-Rao C, Vijayan V, Sharma SK, Ghosh B. Signal transducer and activator of transcription 6 haplotypes and asthma in the Indian population. Am J Respir Cell Mol Biol 2004;31(3):317-21.
43. Nagarkatti R, Ghosh B. Identification of single-nucleotide and repeat polymorphisms in two candidate genes, interleukin 4 receptor (IL4RA) and signal transducer and activator of transcription protein 6 (STAT6), for Th2-mediated diseases. J Hum Genet 2002;47(12):684-7.
44. Buerger H, Gebhardt F, Schmidt H, Beckmann A, Hutmacher K, Simon R, Lelle R, Boecker W, Brandt B. Length and loss of heterozygosity of an intron 1 polymorphic sequence of egfr is related to cytogenetic alterations and epithelial growth factor receptor expression. Cancer Res 2000;60(4):854-7.
45. Travers AA, Klug A. Bending of DNA in Nucleoprotein Complexes. In: Cozzarelli NR, Wang JC, editors. DNA topology and its biological effects. New York: Cold Spring Habour Laboratory Press; 1990. p. 57-106.
46. Searle S, Blackwell JM. Evidence for a functional repeat polymorphism in the promoter of the human NRAMP1 gene that correlates with autoimmune versus infectious disease susceptibility. J Med Genet 1999;36(4):295-9.
47. Shimajiri S, Arima N, Tanimoto A, Murata Y, Hamada T, Wang KY, Sasaguri Y. Shortened microsatellite d(CA)21 sequence down-regulates promoter activity of matrix metalloproteinase 9 gene. FEBS Lett 1999;455(1-2):70-4.
48. Schedel M, Carr D, Klopp N, Woitsch B, Illig T, Stachel D, Schmid I, Fritzsch C, Weiland SK, von Mutius E, Kabesch M. A signal transducer and activator of transcription 6 haplotype influences the regulation of serum IgE levels. J Allergy Clin Immunol 2004;114(5):1100-5.
49. Weidinger S, Klopp N, Wagenpfeil S, Rümmler L, Schedel M, Kabesch M, Schäfer T, Darsow U, Jakob T, Behrendt H, Wichmann HE, Ring J, Illig T. Association of a STAT 6 haplotype with elevated serum IgE levels in a population based cohort of white adults. J Med Genet 2004;41(9):658-63.
50. Pykäläinen M, Kinos R, Valkonen S, Rydman P, Kilpeläinen M, Laitinen LA, Karjalainen J, Nieminen M, Hurme M, Kere J, Laitinen T and Riitta Lahesmaa R. Association analysis of common variants of STAT6, GATA3, and STAT4 to asthma and high serum IgE phenotypes. J Allergy Clin Immunol 2005;115(1):1100-5.
51. Huang CZ, Zou D, Yang J, Qiao HL. Polymorphisms of STAT6 and specific serum IgE levels in patients with penicillin allergy. Int J Clin Pharmacol Ther 2012;50(7):461-7.
52. Stütz AM and Woisetschläger M. Functional synergism of STAT6 with either NF-kB or PU.1 to mediate IL-4-induced activation of IgE germline gene transcription. The Journal of Immunology 1999;163:4383-91.
53. Leung TF, Chan IH, Wong GW, Li CY, Tang NL, Yung E and Lam CW. Association between candidate genes and lung function growth in Chinese asthmatic children. Clinical and Experimental Allergy 2007;37:1480-6.
54. Li CY, Leung TF, Tang NL, Wong GW, Sung YM, Chan IH, Lam CW, Fok TF. STAT6 in17SNP1 and in18SNP1 polymorphisms are not associated with asthma or atopy in Chinese children. J Allergy Clin Immunol 2004;113(Suppl):S205.
55. Wang Q, Bai XT, Xu DQ, Li H, Xu CY, Fang JL. Association of polymorphisms of STAT6 and SO(2) with Chinese childhood asthma: a case-control study. Biomed Environ Sci 2011;24(6):670-7.
56. Granada M, Wilk JB, Tuzova M, Strachan DP, Weidinger S, Albrecht E, Gieger C, Heinrich J, Himes BE, Hunninghake GM, Celedón JC, Weiss ST, Cruikshank WW, Farrer LA, Center DM, O'Connor GT. A genome-wide association study of plasma total IgE concentrations in the Framingham Heart Study. J Allergy Clin Immunol 2012;129(3):840-5.
57. Amoli M, Ollier WE, Hajeer AH. A novel PCR-RFLP assay for the detection of a polymorphism in the 3' of STAT6 gene. Genes Immun 2000;1(5):349-50.
58. Gao PS, Mao XQ, Roberts MH, Arinobu Y, Akaiwa M, Enomoto T, Dake Y, Kawai M, Sasaki S, Hamasaki N, Izuhara K, Shirakawa T, Hopkin JM. Variants of STAT6 (signal transducer and activator of transcription 6) in atopic asthma. J Med Genet 2000;37(5):380-2.
59. Negoro T, Orihara K, Irahara T, Nishiyama H, Hagiwara K, Nishida R, Takagi H, Satoh K, Yamamoto Y, Shimizu S, Hagiwara T, Ishii M, Tanioka T, Nakano Y, Takeda K, Yoshimura I, Iikura Y, Tobe T. Influence of SNPs in cytokine-related genes on the severity of food allergy and atopic eczema in children. Pediatr Allergy Immunol 2006;17(8):583-90.
60. Amoli MM, Hand S, Hajeer AH, Jones KP, Rolf S, Sting C, Davies BH, Ollier WE. Polymorphism in the STAT6 gene encodes risk for nut al lergy. Genes Immun 2002;3(4):220-4.
61. Wu B, Li YF, Xiong HY, Zhang L. Case-control study of STAT6 gene polymorphisms for asthma in Chongqing. Immunology Journal 2006;22(3):308-10.
62. Klein W, Tromm A, Folwaczny C, Hagedorn M, Duerig N, Epplen J, Schmiegel W, Griga T. The G2964A polymorphism of the STAT6 gene in inflammatory bowel disease. Dig Liver Dis 2005;37(3):159-61.
63. Tamura K, Suzuki M, Arakawa H, Tokuyama K, Morikawa A. Linkage and association studies of STAT6 gene polymorphisms and allergic diseases. Int Arch Allergy Immunol 2003;131(1):33-8.
64. Godava M, Kopriva F, Bohmova J, Vodicka R, Dusek L, Cvanova M, Muzik J, Markova M, Schneiderova E, Vrtel R. Association of STAT6 and ADAM33 single nucleotide polymorphisms with asthma bronchiale and IgE level and its possible epigenetic background. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2012;156(3):236-47.
65. Wu X, Li Y, Chen Q, Chen F, Cai P, Wang L, Hu L. Association and gene-gene interactions of eight common single-nucleotide polymorphisms with pediatric asthma in middle china. J Asthma 2010;47(3):238-44.
66. Li Y, Wu B, Xiong H, Zhu C, Zhang L. Polymorphisms of STAT-6, STAT-4 and IFN-gamma genes and the risk of asthma in Chinese population. Respir Med 2007;101(9):1977-81.
67. Martino DJ, Prescott SL. Silent mysteries: epigenetic paradigms could hold the key to conquering the epidemic of allergy and immune disease. Allergy 2010;65:7-15.
68. Biel M, Wascholowski V, Giannis A. Epigenetics - An epicenter of gene regulation: histones and histone-modifying enzymes. Angew Chem Int Ed Engl 2005;44:3186-216.
69. Kim ST, Fields PE, Flavell RA. Demethylation of a specific hypersensitive site in the Th2 locus control region. Proc Natl Acad Sci USA 2007;104:17052-7.
70. Cookson WOCM, Young RP, Sandford AJ, Moffatt MF, Shirakawa T, Sharp PA, Faux JA, Julier C, Le Souef PN, Nakumura Y, Lathrop GM, Hopkin JM. Maternal inheritance of atopic IgE responsiveness on chromosome 11q. Lancet 1992;340:381-4.
71. Kim EG, Shin HJ, Lee CG, Park HY, Kim YK, Park HW, Cho SH, Min KU, Cho ML, Park SH, Lee CW. DNA methylation and not allelic variation regulates STAT6 expression in human T cells. Clin Exp Med 2010;10(3):143-52.
72. Dolinoy DC, Das R, Weidman JR, Jirtle RL. Metastable epialleles, imprinting, and the fetal origins of adult diseases. Pediatr Res 2007;61:30R-37R.
73. Rakyan VK, Chong S, Champ ME, Cuthbert PC, Morgan HD, Luu KV, Whitelaw E. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc Natl Acad Sci USA 2003;100:2538-43.
74. Darcan-Nicolaisen Y, Meinicke H, Fels G, Hegend O, Haberland A, Kühl A, Loddenkemper C, Witzenrath M, Kube S, Henke W, Hamelmann E. Small interfering RNA against transcription factor STAT6 inhibits allergic airway inflammation and hyperreactivity in mice. J Immunol 2009;182(12):7501-8.