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Meta-analysis of genome-wide association studies identifies ten loci influencing allergic sensitization

Nature Genetics volume 45, pages 902–906 (2013)Cite this article

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Abstract

Allergen-specific immunoglobulin E (present in allergic sensitization) has a central role in the pathogenesis of allergic disease. We performed the first large-scale genome-wide association study (GWAS) of allergic sensitization in 5,789 affected individuals and 10,056 controls and followed up the top SNP at each of 26 loci in 6,114 affected individuals and 9,920 controls. We increased the number of susceptibility loci with genome-wide significant association with allergic sensitization from three to ten, including SNPs in or near TLR6, C11orf30, STAT6, SLC25A46, HLA-DQB1, IL1RL1, LPP, MYC, IL2 and HLA-B. All the top SNPs were associated with allergic symptoms in an independent study. Risk-associated variants at these ten loci were estimated to account for at least 25% of allergic sensitization and allergic rhinitis. Understanding the molecular mechanisms underlying these associations may provide new insights into the etiology of allergic disease.

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Figure 1: Manhattan plot for the discovery genome-wide association meta-analysis.
Figure 2: Gene set enrichment map for the 11 significant gene sets from MAGENTA analysis.
Figure 3: Combined impact of risk alleles from the ten genome-wide significant loci on prevalence of allergic sensitization and allergic rhinitis (hay fever) in the population-based Health2006 replication study.

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Acknowledgements

A full list of acknowledgments for each study is given in the Supplementary Note.

Author information

Author notes

  1. Klaus Bønnelykke, Melanie C Matheson, Tune H Pers and Gerard H Koppelman: These authors contributed equally to this work.

  2. Manuel A Ferreira, Hans Bisgaard and A John Henderson: These authors jointly directed this work.

Authors and Affiliations

  1. COPSAC (Copenhagen Prospective Studies on Asthma in Childhood), Health Sciences, University of Copenhagen & Copenhagen University Hospital, Gentofte, Denmark

    Klaus Bønnelykke, Eskil Kreiner-Møller & Hans Bisgaard

  2. Centre for Molecular, Environmental, Genetic and Analytic Epidemiology, University of Melbourne, Melbourne, Victoria, Australia

    Melanie C Matheson & Shyamali C Dharmage

  3. Center for Biological Sequence Analysis, Technical University of Denmark, Lyngby, Denmark

    Tune H Pers & Ramneek Gupta

  4. Division of Endocrinology, Children's Hospital, Boston, Massachusetts, USA

    Tune H Pers & Joel N Hirschhorn

  5. Center for Basic and Translational Obesity Research, Children's Hospital, Boston, Massachusetts, USA

    Tune H Pers

  6. Broad Institute, Cambridge, Massachusetts, USA

    Tune H Pers & Joel N Hirschhorn

  7. School of Social and Community Medicine, University of Bristol, Bristol, UK

    Raquel Granell, Beate St Pourcain, Susan M Ring, Wendy L McArdle, John P Kemp, Nicholas Timpson & A John Henderson

  8. Division of Population Health Sciences & Education, St. George's, University of London, London, UK

    David P Strachan & Wendy L McArdle

  9. Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, UK

    Alexessander Couto Alves, Lachlan Coin & Paul Elliot

  10. Research Centre for Prevention and Health, Glostrup Hospital, Glostrup, Denmark

    Allan Linneberg & Lise L Husemoen

  11. Manchester Academic Health Science Centre, University of Manchester, University Hospital of South Manchester National Health Service (NHS) Foundation Trust, Manchester, UK

    John A Curtin, Angela Simpson & Adnan Custovic

  12. School of Women's and Infants' Health, The University of Western Australia, Crawley, Western Australia, Australia

    Nicole M Warrington & Craig E Pennell

  13. Institute of Epidemiology I, Helmholtz Zentrum München–German Research Center for Environmental Health, Neuherberg, Germany

    Marie Standl, Carla M T Tiesler, Elisabeth Thiering & Joachim Heinrich

  14. Department of Epidemiology, Groningen Research Institute for Asthma and COPD (GRIAC), University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    Marjan Kerkhof

  15. deCODE Genetics, Reykjavik, Iceland

    Ingileif Jonsdottir, Gudmar Thorleifsson, Unnur Thorsteinsdottir & Kari Stefansson

  16. University of Iceland, Reykjavik, Iceland

    Ingileif Jonsdottir, Unnur Thorsteinsdottir & Kari Stefansson

  17. Department of Pediatrics, General Hospital Dr. Josip Bencevic Slavonski Brod, University of Osijek, Osijek, Croatia

    Blazenka K Bukvic & Mario Blekic

  18. Institute of Health Sciences, University of Oulu, Oulu, Finland

    Marika Kaakinen & Marjo-Riitta Jarvelin

  19. Biocenter Oulu, University of Oulu, Oulu, Finland

    Marika Kaakinen & Marjo-Riitta Jarvelin

  20. Center for Applied Genomics, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA

    Patrick Sleimann & Hakon Hakonarsson

  21. Division of Human Genetics, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA

    Patrick Sleimann & Hakon Hakonarsson

  22. Institute of Human Genetics, Helmholtz Zentrum München–German Research Center for Environmental Health, Neuherberg, Germany

    Katharina Schramm

  23. Lung Institute of Western Australia, The University of Western Australia, Perth, Western Australia, Australia

    Svetlana Baltic, Loren Price & Philip J Thompson

  24. Centre for Asthma, Allergy and Respiratory Research, The University of Western Australia, Perth, Western Australia, Australia

    Svetlana Baltic, Loren Price & Philip J Thompson

  25. PathWest Laboratory Medicine of Western Australia, Nedlands, Western Australia, Australia

    Jennie Hui

  26. School of Population Health, The University of Western Australia, Nedlands, Western Australia, Australia

    Jennie Hui

  27. School of Pathology and Laboratory Medicine, The University of Western Australia, Nedlands, Western Australia, Australia

    Jennie Hui

  28. Busselton Population Medical Research Foundation, Sir Charles Gairdner Hospital, Perth, Western Australia, Australia

    Jennie Hui & Alan James

  29. School of Medicine, University of Tasmania, Hobart, Tasmania, Australia

    Eugene H Walters

  30. Queensland Institute of Medical Research, Brisbane, Queensland, Australia

    David L Duffy, Clara S Tang, Grant W Montgomery & Manuel A Ferreira

  31. School of Science and Health, University of Western Sydney, Penrith, New South Wales, Australia

    Graham Jones

  32. Respiratory Medicine, Murdoch Children's Research Institute, Melbourne, Victoria, Australia

    Colin F Robertson

  33. Department of Environmental Health, National Institute for Health and Welfare (THL), Kuopio, Finland

    Juha Pekkanen

  34. Institute of Public Health and Clinical Nutrition, University of Eastern Finland, Kuopio, Finland

    Juha Pekkanen

  35. Department of Clinical Sciences, Obstetrics and Gynecology, Institute of Clinical Medicine, University of Oulu, Oulu, Finland

    Anna-Liisa Hartikainen

  36. Institute for Clinical Diabetology, German Diabetes Center, Leibniz Center for Diabetes Research at Heinrich Heine University Düsseldorf, Düsseldorf, Germany

    Christian Herder

  37. School of Medicine and Pharmacology, The University of Western Australia, Nedlands, Western Australia, Australia

    Alan James

  38. Department of Pulmonary Physiology, West Australian Sleep Disorders Research Institute, Nedlands, Western Australia, Australia

    Alan James

  39. Research Unit of Molecular Epidemiology, Helmholtz Zentrum München–German Research Center for Environmental Health, Neuherberg, Germany

    Melanie Waldenberger

  40. Department of Epidemiology & Preventive Medicine, Monash University, Melbourne, Victoria, Australia

    Michael J Abramson

  41. Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK

    Benjamin P Fairfax & Julian C Knight

  42. Telethon Institute for Child Health Research, The University of Western Australia, Perth, Western Australia, Australia

    Patrick Holt

  43. Centre for Child Health Research, The University of Western Australia, Perth, Western Australia, Australia

    Patrick Holt

  44. Queensland Children's Medical Research Institute, University of Queensland, World Health Organization (WHO) Collaborating Centre for Research on Children's Environmental Health, Brisbane, Queensland, Australia

    Peter Sly

  45. Division of Genetics, Children's Hospital, Boston, Massachusetts, USA

    Joel N Hirschhorn

  46. Department of Genetics, Harvard Medical School, Boston, Massachusetts, USA

    Joel N Hirschhorn

  47. Department of Dermatology, Allergology and Venerology, University Hospital Schleswig-Holstein, Campus Kiel, Kiel, Germany

    Stephan Weidinger

  48. Department of Pulmonology, GRIAC, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    Dirkje S Postma

  49. Department of Epidemiology and Biostatistics, School of Public Health, Medical Research Council–Health Protection Agency (MRC-HPA) Centre for Environment and Health, Imperial College London, London, UK

    Marjo-Riitta Jarvelin

  50. National Institute of Health and Welfare, Oulu, Finland

    Marjo-Riitta Jarvelin

  51. Unit of Primary Care, Oulu University Hospital, Oulu, Finland

    Marjo-Riitta Jarvelin

  52. Department of Pediatric Pulmonology and Pediatric Allergology, Beatrix Children's Hospital, GRIAC, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands

    Gerard H Koppelman

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  1. Klaus Bønnelykke
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  2. Melanie C Matheson
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  3. Tune H Pers
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  4. Raquel Granell
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  5. David P Strachan
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  6. Alexessander Couto Alves
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  7. Allan Linneberg
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  8. John A Curtin
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  9. Nicole M Warrington
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  10. Marie Standl
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  12. Ingileif Jonsdottir
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  13. Blazenka K Bukvic
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  14. Marika Kaakinen
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  15. Patrick Sleimann
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  17. Unnur Thorsteinsdottir
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  18. Katharina Schramm
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  19. Svetlana Baltic
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  20. Eskil Kreiner-Møller
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  21. Angela Simpson
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  22. Beate St Pourcain
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  23. Lachlan Coin
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  24. Jennie Hui
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  25. Eugene H Walters
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  26. Carla M T Tiesler
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  27. David L Duffy
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  28. Graham Jones
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  29. Susan M Ring
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  30. Wendy L McArdle
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  31. Loren Price
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  32. Colin F Robertson
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  33. Juha Pekkanen
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  34. Clara S Tang
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  35. Elisabeth Thiering
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  36. Grant W Montgomery
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  37. Anna-Liisa Hartikainen
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  38. Shyamali C Dharmage
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  39. Lise L Husemoen
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  40. Christian Herder
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  41. John P Kemp
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  42. Paul Elliot
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  43. Alan James
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  44. Melanie Waldenberger
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  45. Michael J Abramson
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  46. Benjamin P Fairfax
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  47. Julian C Knight
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  48. Ramneek Gupta
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  49. Philip J Thompson
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  50. Patrick Holt
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  51. Peter Sly
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  52. Joel N Hirschhorn
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  53. Mario Blekic
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  54. Stephan Weidinger
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  55. Hakon Hakonarsson
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  58. Dirkje S Postma
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  59. Adnan Custovic
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  60. Craig E Pennell
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  61. Marjo-Riitta Jarvelin
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  62. Gerard H Koppelman
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  63. Nicholas Timpson
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  64. Manuel A Ferreira
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  65. Hans Bisgaard
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Consortia

Australian Asthma Genetics Consortium (AAGC)

the EArly Genetics and Lifecourse Epidemiology (EAGLE) Consortium

  • A John Henderson

Contributions

Study-level data analysis: K.B., T.H.P. (meta-analysis and systems biology analyses), R. Granell (meta-analysis), D.P.S., A.C.A. (systems biology analyses), A.L., J.A.C., N.M.W., M.S., M. Kerkhof, B.K.B., M. Kaakinen, P. Sleimann, G.T., K. Schramm, E.K.-M., A.S., L.C., C.S.T., B.P.F., R. Gupta, M.B., S.W., H.H., D.S.P., A.C., G.H.K. and N.T. Study design: K.B., M.C.M., T.H.P., D.P.S., A.L., B.K.B., E.K.-M., A.S., C.F.R., G.W.M., S.C.D., P.E., M.J.A., J.C.K., R. Gupta, P.J.T., J.N.H., M.B., S.W., H.H., J. Heinrich, D.S.P., A.C., C.E.P., M.-R.J., G.H.K., N.T., M.A.F., H.B. and A.J.H. Writing manuscript: K.B., T.H.P., R. Granell, D.P.S., A.C.A., A.L., J.A.C., G.H.K., N.T., M.A.F., H.B. and A.J.H. Data collection: K.B., M.C.M., D.P.S., A.L., I.J., B.K.B., U.T., A.S., J. Hui, E.H.W., D.L.D., G.J., L.P., C.F.R., J.P., E.T., A.-L.H., S.C.D., L.L.H., C.H., A.J., B.P.F., J.C.K., M.J.A., P.J.T., P.H., P. Sly, M.B., H.H., K. Stefansson, J. Heinrich, D.S.P., A.C., M.-R.J., G.H.K., H.B. and A.J.H. Genotyping: K.B., A.L., J.A.C., I.J., P. Sleimann, U.T., S.B., E.K.-M., A.S., B.S.P., C.M.T.T., S.M.R., W.L.M., G.W.M., L.L.H., J.P.K., M.W., H.H., K. Stefansson, A.C., C.E.P., M.-R.J., G.H.K. and H.B. Revising and reviewing manuscript: K.B., M.C.M., T.H.P., R. Granell, D.P.S., A.C.A., A.L., J.A.C., N.M.W., M.S., M. Kerkhof, I.J., B.K.B., M. Kaakinen, P. Sleimann, G.T., U.T., K. Schramm, S.B., E.K.-M., A.S., B.S.P., L.C., J. Hui, E.H.W., C.M.T.T., D.L.D., G.J., S.M.R., W.L.M., L.P., C.F.R., J.P., C.S.T., E.T., G.W.M., A.-L.H., S.C.D., L.L.H., C.H., J.P.K., P.E., A.J., M.W., M.J.A., B.P.F., J.C.K., R. Gupta, P.J.T., P.H., P. Sly, J.N.H., M.B., S.W., H.H., K. Stefansson, J. Heinrich, D.S.P., A.C., C.E.P., M.-R.J., G.H.K., N.T., M.A.F., H.B. and A.J.H.

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Correspondence to Klaus Bønnelykke.

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Competing interests

I.J., G.T., U.T. and K. Stefansson are employees of deCODE Genetics. The other authors declare no competing financial interests.

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Bønnelykke, K., Matheson, M., Pers, T. et al. Meta-analysis of genome-wide association studies identifies ten loci influencing allergic sensitization. Nat Genet 45, 902–906 (2013). https://doi.org/10.1038/ng.2694

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