Polymorphisms related to ORMDL3 are associated with asthma susceptibility, alterations in transcriptional regulation of ORMDL3, and changes in TH2 cytokine levels

Journal of Allergy and Clinical Immunology

Volumn 136, Issue 4, 2015, Pages 893-903.e14

  Schedel, Michaela ^b,c   Michel, Sven ^a,c   Gaertner, Vincent D ^a   Toncheva, Antoaneta A ^a,c   Depner, Martin ^d   Binia, Aristea ^a,m   Schieck, Maximilian ^a,c   Rieger, Marie T ^d   Klopp, Norman ^c,e   Von Berg, Andrea ^f   Bufe, Albrecht ^g   Laub, Otto ^d   Rietschel, Ernst ^h   Heinzmann, Andrea ⁱ   Simma, Burkard ^j   Vogelberg, Christian ^k   Genuneit, Jon ^l   Illig, Thomas ^c,e   Kabesch, Michael ^a,c  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b DEPARTMENT OF MEDICINE   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f Marien Hospital   (Germany)

^g RUHR UNIVERSITY BOCHUM   (Germany)

^h UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

ⁱ UNIVERSITY OF FREIBURG   (Germany)

^j Hospital Feldkirch   (Austria)

^k DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^l UNIVERSITY OF ULM   (Germany)

^m NESTLÉ RESEARCH CENTER   (Switzerland)

more..

Author keywords

association study; Asthma; chromosome 17q21; ORMDL3; polymorphism; promoter activity; TH2 cytokine; transcriptional regulation; upstream stimulatory factor

Indexed keywords

CYTOKINE; INTERLEUKIN 13; INTERLEUKIN 4; LUCIFERASE; OROSOMUCOID; OROSOMUCOID 1 LIKE 3; TH2 CYTOKINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR 1; UPSTREAM STIMULATORY FACTOR 2; MEMBRANE PROTEIN; ORMDL3 PROTEIN, HUMAN;

ALLELE; ALLERGIC ASTHMA; ARTICLE; ASTHMA; CASE CONTROL STUDY; CHROMOSOME 17Q; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENZYME ACTIVITY; EX VIVO STUDY; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; HAPLOTYPE; HUMAN; IN VITRO STUDY; MAJOR CLINICAL STUDY; NONATOPIC ASTHMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION REGULATION; CELL CULTURE; CHILD; CHROMOSOME 17; FEMALE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; GENOTYPE; GERMANY; IMMUNOLOGY; INTERNATIONAL COOPERATION; MALE; METABOLISM; MONONUCLEAR CELL; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; TH1 TH2 BALANCE; TH2 CELL;

ASTHMA; CASE-CONTROL STUDIES; CELLS, CULTURED; CHILD; CHROMOSOMES, HUMAN, PAIR 17; CROSS-SECTIONAL STUDIES; DNA MUTATIONAL ANALYSIS; FEMALE; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; GERMANY; HAPLOTYPES; HUMANS; INTERLEUKIN-13; INTERLEUKIN-4; INTERNATIONAL COOPERATION; LEUKOCYTES, MONONUCLEAR; MALE; MEMBRANE PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; TH1-TH2 BALANCE; TH2 CELLS;

EID: 84942376724     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2015.03.014     Document Type: Article

References (65)

1. M.F. Moffatt, M. Kabesch, L. Liang, A.L. Dixon, D. Strachan, S. Heath, and et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma Nature 448 2007 470 473
2. S. Berlivet, S. Moussette, M. Ouimet, D.J. Verlaan, V. Koka, A. Al Tuwaijri, and et al. Interaction between genetic and epigenetic variation defines gene expression patterns at the asthma-associated locus 17q12-q21 in lymphoblastoid cell lines Hum Genet 131 2012 1161 1171
3. E. Bouzigon, E. Corda, H. Aschard, M.H. Dizier, A. Boland, J. Bousquet, and et al. Effect of 17q21 variants and smoking exposure in early-onset asthma N Engl J Med 359 2008 1985 1994
4. M.A. Ferreira, A.F. McRae, S.E. Medland, D.R. Nyholt, S.D. Gordon, M.J. Wright, and et al. Association between ORMDL3, IL1RL1 and a deletion on chromosome 17q21 with asthma risk in Australia Eur J Hum Genet 19 2011 458 464
5. J.H. Flory, P.M. Sleiman, J.D. Christie, K. Annaiah, J. Bradfield, C.E. Kim, and et al. 17q12-21 variants interact with smoke exposure as a risk factor for pediatric asthma but are equally associated with early-onset versus late-onset asthma in North Americans of European ancestry J Allergy Clin Immunol 124 2009 605 607
6. J. Galanter, S. Choudhry, C. Eng, S. Nazario, J.R. Rodriguez-Santana, J. Casal, and et al. ORMDL3 gene is associated with asthma in three ethnically diverse populations Am J Respir Crit Care Med 177 2008 1194 1200
7. E. Halapi, D.F. Gudbjartsson, G.M. Jonsdottir, U.S. Bjornsdottir, G. Thorleifsson, H. Helgadottir, and et al. A sequence variant on 17q21 is associated with age at onset and severity of asthma Eur J Hum Genet 18 2010 902 908
8. T. Hirota, M. Harada, M. Sakashita, S. Doi, A. Miyatake, K. Fujita, and et al. Genetic polymorphism regulating ORM1-like 3 (Saccharomyces cerevisiae) expression is associated with childhood atopic asthma in a Japanese population J Allergy Clin Immunol 121 2008 769 770
9. T.F. Leung, H.Y. Sy, M.C. Ng, I.H. Chan, G.W. Wong, N.L. Tang, and et al. Asthma and atopy are associated with chromosome 17q21 markers in Chinese children Allergy 64 2009 621 628
10. M.F. Moffatt, I.G. Gut, F. Demenais, D.P. Strachan, E. Bouzigon, S. Heath, and et al. A large-scale, consortium-based genomewide association study of asthma N Engl J Med 363 2010 1211 1221
11. P.M. Sleiman, K. Annaiah, M. Imielinski, J.P. Bradfield, C.E. Kim, E.C. Frackelton, and et al. ORMDL3 variants associated with asthma susceptibility in North Americans of European ancestry J Allergy Clin Immunol 122 2008 1225 1227
12. D.J. Verlaan, S. Berlivet, G.M. Hunninghake, A.M. Madore, M. Lariviere, S. Moussette, and et al. Allele-specific chromatin remodeling in the ZPBP2/GSDMB/ORMDL3 locus associated with the risk of asthma and autoimmune disease Am J Hum Genet 85 2009 377 393
13. A. Lluis, M. Schedel, J. Liu, S. Illi, M. Depner, E. von Mutius, and et al. Asthma-associated polymorphisms in 17q21 influence cord blood ORMDL3 and GSDMA gene expression and IL-17 secretion J Allergy Clin Immunol 127 2011 1587 1594.e6
14. G. Cantero-Recasens, C. Fandos, F. Rubio-Moscardo, M.A. Valverde, and R. Vicente The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress Hum Mol Genet 19 2010 111 121
15. A. Carreras-Sureda, G. Cantero-Recasens, F. Rubio-Moscardo, K. Kiefer, C. Peinelt, B.A. Niemeyer, and et al. ORMDL3 modulates store-operated calcium entry and lymphocyte activation Hum Mol Genet 22 2013 519 530
16. K.J. Hsu, and S.E. Turvey Functional analysis of the impact of ORMDL3 expression on inflammation and activation of the unfolded protein response in human airway epithelial cells Allergy Asthma Clin Immunol 9 2013 4
17. D.J. Todd, A.H. Lee, and L.H. Glimcher The endoplasmic reticulum stress response in immunity and autoimmunity Nat Rev Immunol 8 2008 663 674
18. K. Zhang, and R.J. Kaufman From endoplasmic-reticulum stress to the inflammatory response Nature 454 2008 455 462
19. R.S. Lewis Calcium signaling mechanisms in T lymphocytes Annu Rev Immunol 19 2001 497 521
20. K.S. Weber, M.J. Miller, and P.M. Allen Th17 cells exhibit a distinct calcium profile from Th1 and Th2 cells and have Th1-like motility and NF-AT nuclear localization J Immunol 180 2008 1442 1450
21. M. Miller, A.B. Tam, J.Y. Cho, T.A. Doherty, A. Pham, N. Khorram, and et al. ORMDL3 is an inducible lung epithelial gene regulating metalloproteases, chemokines, OAS, and ATF6 Proc Natl Acad Sci U S A 109 2012 16648 16653
22. S.G. Ha, X.N. Ge, N.S. Bahaie, B.N. Kang, A. Rao, S.P. Rao, and et al. ORMDL3 promotes eosinophil trafficking and activation via regulation of integrins and CD48 Nat Commun 4 2013 2479
23. D.K. Breslow, S.R. Collins, B. Bodenmiller, R. Aebersold, K. Simons, A. Shevchenko, and et al. Orm family proteins mediate sphingolipid homeostasis Nature 463 2010 1048 1053
24. T.S. Worgall, A. Veerappan, B. Sung, B.I. Kim, E. Weiner, R. Bholah, and et al. Impaired sphingolipid synthesis in the respiratory tract induces airway hyperreactivity Sci Transl Med 5 2013 186ra67
25. G.R. Abecasis, D. Altshuler, A. Auton, L.D. Brooks, R.M. Durbin, R.A. Gibbs, and et al. A map of human genome variation from population-scale sequencing Nature 467 2010 1061 1073
26. D.J. Schaid, C.M. Rowland, D.E. Tines, R.M. Jacobson, and G.A. Poland Score tests for association between traits and haplotypes when linkage phase is ambiguous Am J Hum Genet 70 2002 425 434
27. S.K. Weiland, E. von Mutius, T. Hirsch, H. Duhme, C. Fritzsch, B. Werner, and et al. Prevalence of respiratory and atopic disorders among children in the East and West of Germany five years after unification Eur Respir J 14 1999 862 870
28. E. von Mutius, S.K. Weiland, C. Fritzsch, H. Duhme, and U. Keil Increasing prevalence of hay fever and atopy among children in Leipzig, East Germany Lancet 351 1998 862 866
29. S. Michel, L. Liang, M. Depner, N. Klopp, A. Ruether, A. Kumar, and et al. Unifying candidate gene and GWAS approaches in asthma PLoS One 5 2010 e13894
30. M. Schedel, D. Carr, N. Klopp, B. Woitsch, T. Illig, D. Stachel, and et al. A signal transducer and activator of transcription 6 haplotype influences the regulation of serum IgE levels J Allergy Clin Immunol 114 2004 1100 1105
31. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate: a practical and powerful approach to multiple testing J R Stat Soc 57 1995 289 300
32. J.C. Barrett, B. Fry, J. Maller, and M.J. Daly Haploview: analysis and visualization of LD and haplotype maps Bioinformatics 21 2005 263 265
33. L. Excoffier, and M. Slatkin Maximum-likelihood estimation of molecular haplotype frequencies in a diploid population Mol Biol Evol 12 1995 921 927
34. F. Dudbridge Pedigree disequilibrium tests for multilocus haplotypes Genet Epidemiol 25 2003 115 121
35. The 1000 Genomes Project Data. Available at: http://cran.r-project.org/web/packages/haplo.stats/index.html. Accessed April 2014.
36. D.V. Zaykin, P.H. Westfall, S.S. Young, M.A. Karnoub, M.J. Wagner, and M.G. Ehm Testing association of statistically inferred haplotypes with discrete and continuous traits in samples of unrelated individuals Hum Hered 53 2002 79 91
37. Team RC. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Available at: http://www.R-project.org/.
38. L. Hjelmqvist, M. Tuson, G. Marfany, E. Herrero, S. Balcells, and R. Gonzalez-Duarte ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins Genome Biol 3 2002 RESEARCH0027
39. R. Jin, H.G. Xu, W.X. Yuan, L.L. Zhuang, L.F. Liu, L. Jiang, and et al. Mechanisms elevating ORMDL3 expression in recurrent wheeze patients: role of Ets-1, p300 and CREB Int J Biochem Cell Biol 44 2012 1174 1183
40. R. Qiu, Y. Yang, H. Zhao, J. Li, Q. Xin, S. Shan, and et al. Signal transducer and activator of transcription 6 directly regulates human ORMDL3 expression FEBS J 280 2013 2014 2026
41. E. Adam, K.K. Hansen, O. Astudillo Fernandez, L. Coulon, F. Bex, X. Duhant, and et al. The house dust mite allergen Der p 1, unlike Der p 3, stimulates the expression of interleukin-8 in human airway epithelial cells via a proteinase-activated receptor-2-independent mechanism J Biol Chem 281 2006 6910 6923
42. P.G. Gibson, J.L. Simpson, and N. Saltos Heterogeneity of airway inflammation in persistent asthma: evidence of neutrophilic inflammation and increased sputum interleukin-8 Chest 119 2001 1329 1336
43. M.Z. Norzila, K. Fakes, R.L. Henry, J. Simpson, and P.G. Gibson Interleukin-8 secretion and neutrophil recruitment accompanies induced sputum eosinophil activation in children with acute asthma Am J Respir Crit Care Med 161 2000 769 774
44. C.M. Robroeks, G.T. Rijkers, Q. Jobsis, H.J. Hendriks, J.G. Damoiseaux, L.J. Zimmermann, and et al. Increased cytokines, chemokines and soluble adhesion molecules in exhaled breath condensate of asthmatic children Clin Exp Allergy 40 2010 77 84
45. A. Anantharaman, I.J. Lin, J. Barrow, S.Y. Liang, J. Masannat, J. Strouboulis, and et al. Role of helix-loop-helix proteins during differentiation of erythroid cells Mol Cell Biol 31 2011 1332 1343
46. S. Corre, and M.D. Galibert Upstream stimulating factors: highly versatile stress-responsive transcription factors Pigment Cell Res 18 2005 337 348
47. G. Suske The Sp-family of transcription factors Gene 238 1999 291 300
48. W.B. Ball, M. Mukherjee, S. Srivastav, and P.K. Das Leishmania donovani activates uncoupling protein 2 transcription to suppress mitochondrial oxidative burst through differential modulation of SREBP2, Sp1 and USF1 transcription factors Int J Biochem Cell Biol 48 2014 66 76
49. Y. Bu, and I.H. Gelman v-Src-mediated down-regulation of SSeCKS metastasis suppressor gene promoter by the recruitment of HDAC1 into a USF1-Sp1-Sp3 complex J Biol Chem 282 2007 26725 26739
50. Y. Ge, T.L. Jensen, L.H. Matherly, and J.W. Taub Physical and functional interactions between USF and Sp1 proteins regulate human deoxycytidine kinase promoter activity J Biol Chem 278 2003 49901 49910
51. R.L. Clifford, A.E. John, C.E. Brightling, and A.J. Knox Abnormal histone methylation is responsible for increased vascular endothelial growth factor 165a secretion from airway smooth muscle cells in asthma J Immunol 189 2012 819 831
52. C. Deng, Y. Li, S. Liang, K. Cui, T. Salz, H. Yang, and et al. USF1 and hSET1A mediated epigenetic modifications regulate lineage differentiation and HoxB4 transcription PLoS Genet 9 2013 e1003524
53. S. Michel, F. Busato, J. Genuneit, J. Pekkanen, J.C. Dalphin, J. Riedler, and et al. Farm exposure and time trends in early childhood may influence DNA methylation in genes related to asthma and allergy Allergy 68 2013 355 364
54. M.F. Moffatt, M. Kabesch, L. Liang, A.L. Dixon, D. Strachan, S. Heath, and et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma Nature 448 2007 470 473
55. S. Michel, L. Liang, M. Depner, N. Klopp, A. Ruether, A. Kumar, and et al. Unifying candidate gene and GWAS approaches in asthma PLoS One 5 2010 e13894
56. M.F. Moffatt, I.G. Gut, F. Demenais, D.P. Strachan, E. Bouzigon, S. Heath, and et al. A large-scale, consortium-based genomewide association study of asthma N Engl J Med 363 2010 1211 1221
57. S.K. Weiland, E. von Mutius, T. Hirsch, H. Duhme, C. Fritzsch, B. Werner, and et al. Prevalence of respiratory and atopic disorders among children in the East and West of Germany five years after unification Eur Respir J 14 1999 862 870
58. E. von Mutius, S.K. Weiland, C. Fritzsch, H. Duhme, and U. Keil Increasing prevalence of hay fever and atopy among children in Leipzig, East Germany Lancet 351 1998 862 866
59. D.P. Potaczek, S. Michel, V. Sharma, S. Zeilinger, C. Vogelberg, A. von Berg, and et al. Different FCER1A polymorphisms influence IgE levels in asthmatics and non-asthmatics Pediatr Allergy Immunol 24 2013 441 449
60. M. Schedel, L.A. Pinto, B. Schaub, P. Rosenstiel, D. Cherkasov, L. Cameron, and et al. IRF-1 gene variations influence IgE regulation and atopy Am J Respir Crit Care Med 177 2008 613 621
61. T. Matsukawa, Y. Inoue, Y. Oishi, H. Kato, and T. Noguchi Up-regulation of upstream stimulatory factors by protein malnutrition and its possible role in regulation of the IGF-binding protein-1 gene Endocrinology 142 2001 4643 4651
62. T.D. LeVan, J.W. Bloom, T.J. Bailey, C.L. Karp, M. Halonen, F.D. Martinez, and et al. A common single nucleotide polymorphism in the CD14 promoter decreases the affinity of Sp protein binding and enhances transcriptional activity J Immunol 167 2001 5838 5844
63. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method Methods 25 2001 402 408
64. Team RC. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Available at: http://www.R-project.org/.
65. M. Schedel, D. Carr, N. Klopp, B. Woitsch, T. Illig, D. Stachel, and et al. A signal transducer and activator of transcription 6 haplotype influences the regulation of serum IgE levels J Allergy Clin Immunol 114 2004 1100 1105