The Journal of Allergy and Clinical Immunology
Volume 124, Issue 2 , Pages 222-229 , August 2009

A thymic stromal lymphopoietin gene variant is associated with asthma and airway hyperresponsiveness

  • Jian-Qing He, MD

      Affiliations

    • James Hogg Imaging, Cell Analysis, and Phenotyping Toward Understanding Responsive, Reparative, Remodelling, and Recombinant Events (iCAPTURE) Centre, University of British Columbia, Vancouver, British Columbia, Canada
    • ,
  • Teal S. Hallstrand, MD, MPH

      Affiliations

    • Department of Medicine, Division of Pulmonary and Critical Care, University of Washington, Seattle, Wash
    • ,
  • Darryl Knight, PhD

      Affiliations

    • James Hogg Imaging, Cell Analysis, and Phenotyping Toward Understanding Responsive, Reparative, Remodelling, and Recombinant Events (iCAPTURE) Centre, University of British Columbia, Vancouver, British Columbia, Canada
    • Department of Anesthesiology, Pharmacology and Therapeutics, University of British Columbia, Vancouver, British Columbia, Canada
    • ,
  • Moira Chan-Yeung, MD

      Affiliations

    • Occupational and Environmental Lung Disease Unit, University of British Columbia, Vancouver, British Columbia, Canada
    • ,
  • Andrew Sandford, PhD

      Affiliations

    • James Hogg Imaging, Cell Analysis, and Phenotyping Toward Understanding Responsive, Reparative, Remodelling, and Recombinant Events (iCAPTURE) Centre, University of British Columbia, Vancouver, British Columbia, Canada
    • Division of Respiratory Medicine, Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada
    • ,
  • Ben Tripp, BSs

      Affiliations

    • James Hogg Imaging, Cell Analysis, and Phenotyping Toward Understanding Responsive, Reparative, Remodelling, and Recombinant Events (iCAPTURE) Centre, University of British Columbia, Vancouver, British Columbia, Canada
    • ,
  • David Zamar, MSc

      Affiliations

    • James Hogg Imaging, Cell Analysis, and Phenotyping Toward Understanding Responsive, Reparative, Remodelling, and Recombinant Events (iCAPTURE) Centre, University of British Columbia, Vancouver, British Columbia, Canada
    • ,
  • Yohan Bossé, PhD

      Affiliations

    • Institut universitaire de cardiologie et de pneumologie de Québec, Quebec, Canada
    • Department of Medicine, Laval University Hospital Research Center, Quebec City, Quebec, Canada
    • ,
  • Anita L. Kozyrskyj, PhD

      Affiliations

    • Department of Pediatrics, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada
    • Department of Pediatrics and Child Health, Faculty of Medicine, University of Manitoba, Winnipeg, Manitoba, Canada
    • ,
  • Alan James, MD

      Affiliations

    • West Australian Sleep Disorders Research Institute, Sir Charles Gairdner Hospital, Perth, Australia
    • ,
  • Catherine Laprise, PhD

      Affiliations

    • Département des Sciences Fondamentales, Université du Québec à Chicoutimi, Quebec, Canada
    • Université de Montréal Community Genomic Medicine Center, Chicoutimi Hospital, Canada
    • ,
  • Denise Daley, PhD

      Affiliations

    • James Hogg Imaging, Cell Analysis, and Phenotyping Toward Understanding Responsive, Reparative, Remodelling, and Recombinant Events (iCAPTURE) Centre, University of British Columbia, Vancouver, British Columbia, Canada
    • Division of Respiratory Medicine, Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada
    • Corresponding Author InformationReprint requests: Denise Daley, PhD, UBC James Hogg iCAPTURE Centre, 1081 Burrard Street, Vancouver, BC, Canada V6Z 1Y6.

Received 10 December 2008 ,Revised 6 April 2009 ,Accepted 8 April 2009.

References 

  1. Strachan DP. Hay fever, hygiene, and household size. Br Med J. 1989;299:1259–1260
  2. Wills-Karp M, Santeliz J, Karp CL. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol. 2001;1:69–75
  3. Ziegler SF, Liu YJ. Thymic stromal lymphopoietin in normal and pathogenic T cell development and function. Nat Immunol. 2006;7:709–714
  4. Liu YJ, Soumelis V, Watanabe N, Ito T, Wang YH, Malefyt Rde W, et al. TSLP: an epithelial cell cytokine that regulates T cell differentiation by conditioning dendritic cell maturation. Annu Rev Immunol. 2007;25:193–219
  5. Liu YJ. Thymic stromal lymphopoietin: master switch for allergic inflammation. J Exp Med. 2006;203:269–273
  6. Park LS, Martin U, Garka K, Gliniak B, Di Santo JP, Muller W, et al. Cloning of the murine thymic stromal lymphopoietin (TSLP) receptor: formation of a functional heteromeric complex requires interleukin 7 receptor. J Exp Med. 2000;192:659–670
  7. Tonozuka Y, Fujio K, Sugiyama T, Nosaka T, Hirai M, Kitamura T. Molecular cloning of a human novel type I cytokine receptor related to delta1/TSLPR. Cytogenet Cell Genet. 2001;93:23–25
  8. Shamim Z, Muller K, Svejgaard A, Poulsen LK, Bodtger U, Ryder LP. Association between genetic polymorphisms in the human interleukin-7 receptor alpha-chain and inhalation allergy. Int J Immunogenet. 2007;34:149–151
  9. Zhou B, Comeau MR, De Smedt T, Liggitt HD, Dahl ME, Lewis DB, et al. Thymic stromal lymphopoietin as a key initiator of allergic airway inflammation in mice. Nat Immunol. 2005;6:1047–1053
  10. Yoo J, Omori M, Gyarmati D, Zhou B, Aye T, Brewer A, et al. Spontaneous atopic dermatitis in mice expressing an inducible thymic stromal lymphopoietin transgene specifically in the skin. J Exp Med. 2005;202:541–549
  11. Taneda S, Segerer S, Hudkins KL, Cui Y, Wen M, Segerer M, et al. Cryoglobulinemic glomerulonephritis in thymic stromal lymphopoietin transgenic mice. Am J Pathol. 2001;159:2355–2369
  12. Kowalewska J, Muhlfeld AS, Hudkins KL, Yeh MM, Farr AG, Ravetch JV, et al. Thymic stromal lymphopoietin transgenic mice develop cryoglobulinemia and hepatitis with similarities to human hepatitis C liver disease. Am J Pathol. 2007;170:981–989
  13. Headley MB, Zhou B, Shih WX, Aye T, Comeau MR, Ziegler SF. TSLP conditions the lung immune environment for the generation of pathogenic innate and antigen-specific adaptive immune responses. J Immunol. 2009;182:1641–1647
  14. Ying S, O'Connor B, Ratoff J, Meng Q, Mallett K, Cousins D, et al. Thymic stromal lymphopoietin expression is increased in asthmatic airways and correlates with expression of Th2-attracting chemokines and disease severity. J Immunol. 2005;174:8183–8190
  15. Kato A, Favoreto S, Avila PC, Schleimer RP. TLR3- and Th2 cytokine-dependent production of thymic stromal lymphopoietin in human airway epithelial cells. J Immunol. 2007;179:1080–1087
  16. Lemanske RF, Busse WW. Asthma: factors underlying inception, exacerbation, and disease progression. J Allergy Clin Immunol. 2006;117(2 Suppl Mini-Primer):S456–S461
  17. Hunninghake GM, Lasky-Su J, Soto-Quiros ME, Avila L, Liang C, Lake SL, et al. Sex-stratified linkage analysis identifies a locus for IgE to cockroach in female Costa Ricans. Am J Respir Crit Care Med. 2008;15:177:830–836
  18. Chan-Yeung M, Manfreda J, Dimich-Ward H, Ferguson A, Watson W, Becker A. A randomized controlled study on the effectiveness of a multifaceted intervention program in the primary prevention of asthma in high-risk infants. Arch Pediatr Adolesc Med. 2000;154:657–663
  19. Chan-Yeung M, Ferguson A, Watson W, Dimich-Ward H, Rousseau R, Lilley M, et al. The Canadian Childhood Asthma Primary Prevention Study: outcomes at 7 years of age. J Allergy Clin Immunol. 2005;116:49–55
  20. Kozyrskyj AL, Mai XM, McGrath P, Hayglass KT, Becker AB, Macneil B. Continued exposure to maternal distress in early life is associated with an increased risk of childhood asthma. Am J Respir Crit Care Med. 2008;177:142–147
  21. Mai XM, Becker AB, Sellers EA, Liem JJ, Kozyrskyj AL. The relationship of breast-feeding, overweight, and asthma in preadolescents. J Allergy Clin Immunol. 2007;120:551–556
  22. Begin P, Tremblay K, Daley D, Lemire M, Claveau S, Salesse C, et al. Association of urokinase-type plasminogen activator with asthma and atopy. Am J Respir Crit Care Med. 2007;175:1109–1116
  23. Laprise C, Sladek R, Ponton A, Bernier MC, Hudson TJ, Laviolette M. Functional classes of bronchial mucosa genes that are differentially expressed in asthma. BMC Genomics. 2004;5:21
  24. Poon AH, Laprise C, Lemire M, Hudson TJ, Schurr E. NRAMP1 is not associated with asthma, atopy, and serum immunoglobulin E levels in the French Canadian population. Genes Immun. 2005;6:519–527
  25. Poon AH, Laprise C, Lemire M, Montpetit A, Sinnett D, Schurr E, et al. Association of vitamin D receptor genetic variants with susceptibility to asthma and atopy. Am J Respir Crit Care Med. 2004;170:967–973
  26. Raby BA, Lazarus R, Silverman EK, Lake S, Lange C, Wjst M, et al. Association of vitamin D receptor gene polymorphisms with childhood and adult asthma. Am J Respir Crit Care Med. 2004;170:1057–1065
  27. Tremblay K, Provost V, Lemire M, Page N, Sandford A, Hudson T, et al. Association study between the CX3CR1 gene and asthma: a new candidate gene identified by microarray technology. Proc Am Thorac Soc. 2005;2:A30
  28. James AL, Palmer LJ, Kicic E, Maxwell PS, Lagan SE, Ryan GF, et al. Decline in lung function in the Busselton Health Study: the effects of asthma and cigarette smoking. Am J Respir Crit Care Med. 2005;171:109–114
  29. James AL, Knuiman MW, Bartholomew HC, Musk AB. What can Busselton population health surveys tell us about asthma in older people?. Med J Aust. 2005;183(1 Suppl):S17–S19
  30. Bremner PR, de Klerk NH, Ryan GF, James AL, Musk M, Murray C, et al. Respiratory symptoms and lung function in aborigines from tropical Western Australia. Am J Respir Crit Care Med. 1998;158:1724–1729
  31. Moffatt MF, Kabesch M, Liang L, Dixon AL, Strachan D, Heath S, et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature. 2007;448:470–473
  32. Godfrey S, Springer C, Bar-Yishay E, Avital A. Cut-off points defining normal and asthmatic bronchial reactivity to exercise and inhalation challenges in children and young adults. Eur Respir J. 1999;14:659–668
  33. Godfrey S. Bronchial hyper-responsiveness in children. Paediatr Respir Rev. 2000;1:148–155
  34. Carlson CS, Eberle MA, Rieder MJ, Yi Q, Kruglyak L, Nickerson DA. Selecting a maximally informative set of single-nucleotide polymorphisms for association analyses using linkage disequilibrium. Am J Hum Genet. 2004;74:106–120
  35. Tremblay K, Lemire M, Provost V, Pastinen T, Renaud Y, Sandford AJ, et al. Association study between the CX3CR1 gene and asthma. Genes Immun. 2006;7:632–639
  36. Shen R, Fan JB, Campbell D, Chang W, Chen J, Doucet D, et al. High-throughput SNP genotyping on universal bead arrays. Mutat Res. 2005;573:70–82
  37. Lincoln MR, Montpetit A, Cader MZ, Saarela J, Dyment DA, Tiislar M, et al. A predominant role for the HLA class II region in the association of the MHC region with multiple sclerosis. Nat Genet. 2005;37:1108–1112
  38. Dudbridge F. Pedigree disequilibrium tests for multilocus haplotypes. Genet Epidemiol. 2003;25:115–121
  39. Dudbridge F. Likelihood-based association analysis for nuclear families and unrelated subjects with missing genotype data. Hum Hered. 2008;66:87–98
  40. Spielman RS, McGinnis RE, Ewens WJ. Transmission test for linkage disequilibrium: the insulin gene region and insulin-dependent diabetes mellitus (IDDM). Am J Hum Genet. 1993;52:506–516
  41. Curtis D, Sham PC. A note on the application of the transmission disequilibrium test when a parent is missing. Am J Hum Genet. 1995;56:811–812
  42. Nyholt DR. A simple correction for multiple testing for single-nucleotide polymorphisms in linkage disequilibrium with each other. Am J Hum Genet. 2004;74:765–769
  43. Neale BM, Sham PC. The future of association studies: gene-based analysis and replication. Am J Hum Genet. 2004;75:353–362
  44. Ober C, Hoffjan S. Asthma genetics 2006: the long and winding road to gene discovery. Genes Immun. 2006;7:95–100
  45. Li J, Ji L. Adjusting multiple testing in multilocus analyses using the eigenvalues of a correlation matrix. Heredity. 2005;95:221–227
  46. Daley D, Lemire M, Akhabir L, Chan-Yeung M, He JQ, McDonald T, et al. Analyses of associations with asthma in four asthma population samples from Canada and Australia. Hum Genet. 2009;125:445–459
  47. Li M, Hener P, Zhang Z, Kato S, Metzger D, Chambon P. Topical vitamin D3 and low-calcemic analogs induce thymic stromal lymphopoietin in mouse keratinocytes and trigger an atopic dermatitis. Proc Natl Acad Sci U S A. 2006;103:11736–11741
  48. Allakhverdi Z, Comeau MR, Jessup HK, Yoon BR, Brewer A, Chartier S, et al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J Exp Med. 2007;204:253–258
  49. Conde L, Vaquerizas JM, Dopazo H, Arbiza L, Reumers J, Rousseau F, et al. PupaSuite: finding functional single nucleotide polymorphisms for large-scale genotyping purposes. Nucleic Acids Res. 2006;34(Web Server Issue):W621–W625
  50. Harada M, Hirota T, Jodo AI, Doi S, Kameda M, Fujita K, et al. Functional analysis of the thymic stromal lymphopoietin variants in human bronchial epithelial cells. Am J Respir Cell Mol Biol. 2009;40:368–374
  51. Pearce N, Ait-Khaled N, Beasley R, Mallol J, Keil U, Mitchell E, et al. Worldwide trends in the prevalence of asthma symptoms: phase III of the International Study of Asthma and Allergies in Childhood (ISAAC). Thorax. 2007;62:758–766
  52. Vonk JM, Boezen HM. Predicting adult asthma in childhood. Curr Opin Pulm Med. 2006;12:42–47
  53. Ito T, Wang YH, Duramad O, Hori T, Delespesse GJ, Watanabe N, et al. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med. 2005;202:1213–1223
  54. Seshasayee D, Lee WP, Zhou M, Shu J, Suto E, Zhang J, et al. In vivo blockade of OX40 ligand inhibits thymic stromal lymphopoietin driven atopic inflammation. J Clin Invest. 2007;117:3868–3878
  55. Liu YJ. Thymic stromal lymphopoietin and OX40 ligand pathway in the initiation of dendritic cell-mediated allergic inflammation. J Allergy Clin Immunol. 2007;120:238–244quiz 45-46
  56. Wang YH, Liu YJ. OX40-OX40L interactions: a promising therapeutic target for allergic diseases?. J Clin Invest. 2007;117:3655–3657

 Supported by AllerGen, a National Centre of Excellence Network (Canada); the Canadian Institutes of Health Research; the Institutes of Gender and Health; British Columbia Lung Association; Génome Québec; and the Respiratory Health Network of the Fonds de la Recherche en Santé du Québec. The 1994 Busselton follow-up study was funded by Healthway, Australia. J.-Q.H. is the recipient of a Michael Smith Foundation for Health Research Doctoral Award and an Izaak Walton Killam Memorial Scholarship Award. D.K. is a Canada Research Chair, a recipient of a Michael Smith Foundation Scholarship and the William Thurlbeck Distinguished Research Award. A.J. is a recipient of a National Health and Medical Research Council of Australia Practitioner Fellowship. Y.B. and D.D. were recipients of fellowship awards (Canadian Institutes of Health Research), and A.L.K. is a recipient of a New Investigator Award (Canadian Institutes of Health Research). D.D. is the recipient of a Michael Smith Foundation Career Scholar Award. D.D., C.L., and A.S. hold Canadian Research Chair appointments. This work was also supported by the National Health and Medical Research Council of Australia (303145, 458513), the Child Health Research Foundation of Western Australia, and the Asthma Foundation of Western Australia.

 Disclosure of potential conflict of interest: D. Daley receives grant support from AllerGen and the Canadian Institutes of Health Research. T. S. Hallstrand is on the speakers' bureau for Merck and Schering-Plough, is a consultant for Merck, and receives grant support from the National Institutes of Health, the American Lung Foundation, the Firland Foundation, and Novartis. D. Knight receives grant support from Centocor and Sepracor. A. Sandford receives grant support from the British Columbia Lung Association and the Canadian Institutes of Health Research. Y. Bossé receives grant support from the Québec Institute of Cardiology, Fonds de la Recherche en Santé du Québec, the Heart and Stroke Foundation, and the Respiratory Health Network of the Fonds de la Recherche en Santé du Québec. The rest of the authors have declared that they have no conflict of interest.

PII: S0091-6749(09)00643-5

doi: 10.1016/j.jaci.2009.04.018

The Journal of Allergy and Clinical Immunology
Volume 124, Issue 2 , Pages 222-229 , August 2009

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