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Multiancestry association study identifies new asthma risk loci that colocalize with immune-cell enhancer marks

Nature Genetics volume 50, pages 42–53 (2018)Cite this article

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Abstract

We examined common variation in asthma risk by conducting a meta-analysis of worldwide asthma genome-wide association studies (23,948 asthma cases, 118,538 controls) of individuals from ethnically diverse populations. We identified five new asthma loci, found two new associations at two known asthma loci, established asthma associations at two loci previously implicated in the comorbidity of asthma plus hay fever, and confirmed nine known loci. Investigation of pleiotropy showed large overlaps in genetic variants with autoimmune and inflammatory diseases. The enrichment in enhancer marks at asthma risk loci, especially in immune cells, suggested a major role of these loci in the regulation of immunologically related mechanisms.

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Fig. 1: Manhattan plots of the results of European-ancestry and multiancestry random-effects meta-analyses of asthma risk.
Fig. 2: GRAIL circle plot of connectivity among genes at asthma risk loci.

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Acknowledgements

We thank all participants who provided data for each study and also thank our valued colleagues who contributed to data collection and phenotypic characterization of clinical samples, genotyping, and analysis of individual datasets. Detailed acknowledgments and funding for individual studies can be found in the Supplementary Note.

Author information

Author notes

  1. A full list of members and affiliations appears in the Supplementary Note.

  2. Florence Demenais, Patricia Margaritte-Jeannin, Kathleen C. Barnes, William O. C. Cookson, Miriam F. Moffatt, Carole Ober and Dan Nicolae contributed equally to this work.

Authors and Affiliations

  1. Genetic Variation and Human Diseases Unit (UMR-946), Institut National de la Santé et de la Recherche Médicale (INSERM), Paris, France

    Florence Demenais, Patricia Margaritte-Jeannin, Emmanuelle Bouzigon, Myriam Brossard, Sébastien Letort, Hamida Mohamdi & Amaury Vaysse

  2. Institut Universitaire d’Hématologie, Université Paris Diderot, Université Sorbonne Paris Cité, Paris, France

    Florence Demenais, Patricia Margaritte-Jeannin, Emmanuelle Bouzigon, Myriam Brossard, Sébastien Letort, Hamida Mohamdi & Amaury Vaysse

  3. Division of Biomedical Informatics and Personalized Medicine, Colorado Center for Personalized Medicine, University of Colorado, Denver, CO, USA

    Kathleen C. Barnes

  4. Section of Genomic Medicine, National Heart and Lung Institute, London, UK

    William O. C. Cookson & Miriam F. Moffatt

  5. Cologne Center for Genomics and Center for Molecular Medicine Cologne (CMMC), University of Cologne, Cologne, Germany

    Janine Altmüller

  6. School of Women’s and Infants’ Health, University of Western Australia, Perth, Western Australia, Australia

    Wei Ang & Craig E. Pennell

  7. Departments of Medicine and Epidemiology, Columbia University, New York, NY, USA

    R. Graham Barr & Kathleen M. Donohue

  8. Division of Genetic Epidemiology, Department of Epidemiology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA

    Terri H. Beaty

  9. Department of Pediatrics and Child Health, University of Manitoba, Winnipeg, Manitoba, Canada

    Allan B. Becker

  10. Department of the Diagnostic Genomics Laboratory, PathWest Laboratory Medicine, Queen Elizabeth II Medical Centre, Nedlands, Western Australia, Australia

    John Beilby & Jennie Hui

  11. Copenhagen Prospective Studies on Asthma in Childhood, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark

    Hans Bisgaard, Klaus Bønnelykke, Eskil Kreiner & Johannes Waage

  12. Department of Medicine, Landspitali, National University Hospital of Iceland, Reykjavik, Iceland

    Unnur Steina Bjornsdottir

  13. Center for Genomics, Wake Forest University School of Medicine, Winston-Salem, NC, USA

    Eugene Bleecker & Deborah Meyers

  14. Department of Biological Psychology, Amsterdam Public Health Research Institute, Vrjie Universiteit, Amsterdam, The Netherlands

    Dorret I. Boomsma, Jouke Hottenga, Hamdi Mbarek & Gonneke Willemsen

  15. University of Leicester, Institute for Lung Health, Glenfield Hospital, Leicester, UK

    Christopher E. Brightling

  16. Department of Respiratory Medicine, Ghent University Hospital, Ghent, Belgium

    Guy G. Brusselle

  17. Department of Epidemiology, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Guy G. Brusselle, Albert Hofman, Lies Lahousse, Daan W. Loth & Bruno H. Stricker

  18. Department of Respiratory Medicine, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Guy G. Brusselle

  19. Department of Bioengineering & Therapeutic Sciences and Medicine, University of California, San Francisco, San Francisco, CA, USA

    Esteban Burchard

  20. Division of Pulmonary, Allergy and Critical Care, College of Physicians and Surgeons, Columbia University, New York, NY, USA

    Kristin M. Burkart

  21. National Heart and Lung Institute, Imperial College London, London, UK

    Andrew Bush, Kian Fan Chung & Deborah Jarvis

  22. Royal Brompton Harefield National Health Service (NHS) Foundation Trust, London, UK

    Andrew Bush

  23. Department of Medicine, University of British Columbia, Vancouver, British Columbia, Canada

    Moira Chan-Yeung, Denise Daley & Julie E. Park

  24. Biomedical Research Unit, Royal Brompton & Harefield National Health Service (NHS) Trust, London, UK

    Kian Fan Chung

  25. Department of Epidemiology and Biostatistics, Imperial College London, London, UK

    Alexessander Couto Alves & Adaikalavan Ramasamy

  26. Division of Infection, Immunity and Respiratory Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, Manchester Academic Health Science Centre, University of Manchester, Manchester, UK

    John A. Curtin & Angela Simpson

  27. Department of Paediatrics, Imperial College London, London, UK

    Adnan Custovic

  28. Centre for Heart and Lung Innovation, University of British Columbia, Vancouver, BC, Canada

    Denise Daley

  29. Department of Pediatrics, Division of Respiratory Medicine, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Johan C. de Jongste

  30. Hospital Infantil de Mexico Federico Gomez, Mexico City, Mexico

    Blanca E. Del-Rio-Navarro

  31. Department of Pediatrics, Division of Respiratory Medicine, and Department of Pediatrics, Division of Neonatology, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Liesbeth Duijts

  32. Department of Medicine, University of California, San Francisco, San Francisco, CA, USA

    Celeste Eng & Dara G. Torgerson

  33. Department of General Practice and Primary Health Care, University of Helsinki and Helsinki University Hospital, Helsinki, Finland

    Johan G. Eriksson

  34. Division of Cardiovascular Medicine, Radcliffe Department of Medicine, University of Oxford, Oxford, UK

    Martin Farrall

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

    Martin Farrall

  36. Institute of Biochemistry and Genetics, Ufa Scientific Center of the Russian Academy of Sciences, Ufa, Russian Federation

    Yuliya Fedorova, Alexandra S. Karunas & Elza Khusnutdinova

  37. Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark

    Bjarke Feenstra, Frank Geller & Mads Melbye

  38. Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia

    Manuel A. Ferreira

  39. Population Genetics Laboratory, Research Institute of Medical Genetics, Tomsk NRMC, Tomsk, Russian Federation

    Maxim B. Freidin & Valery P. Puzyrev

  40. Divisions of Genetics and Endocrinology, Children’s Hospital, Boston, MA, USA

    Zofia Gajdos & Sailaja Vedantam

  41. Broad Institute, Cambridge, MA, USA

    Zofia Gajdos, Joel N. Hirschhorn, Cameron D. Palmer & Sailaja Vedantam

  42. Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

    Jim Gauderman, Frank Gilliland & Muhammad T. Salam

  43. Division of Environmental Epidemiology, Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands

    Ulrike Gehring, Dick Heederik & Inge M. Wouters

  44. Institute of Epidemiology and Medical Biometry, Ulm University, Ulm, Germany

    Jon Genuneit

  45. Department of Medicine, University of Washington, Seattle, WA, USA

    Sina A. Gharib & Guo Li

  46. Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, UK

    Raquel Granell & John Henderson

  47. MRC Integrative Epidemiology Unit, University of Bristol, Bristol, UK

    Raquel Granell & John Henderson

  48. Asthma and Airway Disease Research Center and BIO5 Institute, University of Arizona, Tucson, AZ, USA

    Penelope E. Graves & Fernando J. Martinez

  49. deCODE genetics, Amgen Inc., Reykjavik, Iceland

    Daniel F. Gudbjartsson, Ingileif Jonsdottir, Kari Stefansson, Gudmar Thorleifsson & Unnur Thorsteinsdottir

  50. School of Engineering and Natural Sciences, University of Iceland, Reykjavik, Iceland

    Daniel F. Gudbjartsson

  51. Skin and Allergy Hospital, University of Helsinki, Helsinki, Finland

    Tari Haahtela

  52. Department of Epidemiology, University of Washington, Seattle, WA, USA

    Susan R. Heckbert

  53. Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, University Hospital in Munich, Munich, Germany

    Joachim Heinrich

  54. Institute of Epidemiology I, Helmholtz Zentrum München, German Research Centre for Environmental Health, Neuherberg, Germany

    Joachim Heinrich, Marie Standl & Carla M. T. Tiesler

  55. National Institute for Health and Welfare (THL), Helsinki, Finland

    Markku Heliövaara, Pekka Jousilahti, Mikko Kuokkanen & Veikko Salomaa

  56. Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania, Philadelphia, PA, USA

    Blanca E. Himes

  57. Health Center, Department of Internal Medicine, Keio University, Tokyo, Japan

    Hiroshi Hirose

  58. Division of Endocrinology and Center for Basic and Translational Obesity Research, Boston Children’s Hospital, Boston, MA, USA

    Joel N. Hirschhorn & Cameron D. Palmer

  59. Departments of Pediatrics and Genetics, Harvard Medical School, Boston, MA, USA

    Joel N. Hirschhorn

  60. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Albert Hofman & Liming Liang

  61. Cell Biology Telethon Kids Institute, University of Western Australia, Subiaco, Western Australia, Australia

    Patrick Holt

  62. Ontario Institute for Cancer Research, Toronto, Ontario, Canada

    Thomas J. Hudson

  63. AbbVie Inc., Redwood City, CA, USA

    Thomas J. Hudson

  64. Busselton Population Medical Research Institute, Perth, Western Australia, Australia

    Jennie Hui

  65. School of Population and Global Health, University of Western Australia, Nedlands, Western Australia, Australia

    Jennie Hui

  66. Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Basel, Switzerland

    Medea Imboden, Ashish Kumar & Nicole Probst-Hensch

  67. University of Basel, Basel, Switzerland

    Medea Imboden, Ashish Kumar & Nicole Probst-Hensch

  68. Department of Biology, Medical Genetics and Ecology, Kursk State Medical University, Kursk, Russian Federation

    Vladimir Ivanov, Alexey Polonikov & Maria Solodilova

  69. The Generation R Study Group, Department of Pediatrics and Department of Epidemiology, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Vincent W. V. Jaddoe

  70. Department of Pulmonary Physiology and Sleep Medicine, Busselton Population Medical Research Institute, Sir Charles Gairdner Hospital, Nedlands, Western Australia, Australia

    Alan James

  71. School of Medicine and Pharmacology, University of Western Australia, Crawley, Western Australia, Australia

    Alan James

  72. Department of Medical Sciences: Respiratory, Allergy & Sleep Research, Uppsala University, Uppsala, Sweden

    Christer Janson

  73. Department of Epidemiology and Biostatistics, MRC–PHE Centre for Environment & Health, School of Public Health, Imperial College London, London, UK

    Marjo-Riitta Jarvelin

  74. Center for Life Course Health Research, Faculty of Medicine, University of Oulu, Oulu, Finland

    Marjo-Riitta Jarvelin

  75. Biocenter Oulu, University of Oulu, Oulu, Finland

    Marjo-Riitta Jarvelin

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

    Marjo-Riitta Jarvelin

  77. MRC–PHE Centre for Environment and Health, Imperial College London, London, UK

    Deborah Jarvis

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

    Graham Jones

  79. Faculty of Medicine, University of Iceland, Reykjavik, Iceland

    Ingileif Jonsdottir, Kari Stefansson & Unnur Thorsteinsdottir

  80. Department of Pediatric Pneumology and Allergy, University Children’s Hospital Regensburg (KUNO), Regensburg, Germany

    Michael Kabesch & Sven Michel

  81. Department of Clinical Physiology, University of Tampere and Tampere University Hospital, Tampere, Finland

    Mika Kähönen

  82. Department of Anesthesiology, Perioperative and Pain Medicine, Division of Critical Care Medicine, Boston Children’s Hospital, Boston, MA, USA

    David B. Kantor

  83. Department of Anaesthesia, Harvard Medical School, Boston, MA, USA

    David B. Kantor

  84. Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russian Federation

    Alexandra S. Karunas & Elza Khusnutdinova

  85. University of Groningen, University Medical Center Groningen, Department of Pediatric Pulmonology and Pediatric Allergology, Beatrix Children’s Hospital, Groningen, The Netherlands

    Gerard H. Koppelman

  86. Groningen Research Institute for Asthma and COPD (GRIAC), Groningen, The Netherlands

    Gerard H. Koppelman, Maartje A. E. Nieuwenhuis, Dirkje S. Postma & Judith M. Vonk

  87. Department of Pediatrics, University of Alberta, Edmonton, Alberta, Canada

    Anita L. Kozyrskyj

  88. RIKEN Center for Integrative Medical Sciences, Yokohama, Japan

    Michiaki Kubo, Atsushi Takahashi & Tatsuhiko Tsunoda

  89. Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, USA

    Rajesh Kumar

  90. Divison of Allergy and Clinical Immunology, Department of Pediatrics, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

    Rajesh Kumar

  91. Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden

    Ashish Kumar, Erik Melén, Göran Pershagen & Magnus Wickman

  92. Institute for Molecular Medicine Finland (FIMM), University of Helsinki, Helsinki, Finland

    Mikko Kuokkanen, Aarno Palotie & Elisabeth Widén

  93. Pharmaceutical Care Unit, Faculty of Pharmaceutical Sciences, Ghent University, Ghent, Belgium

    Lies Lahousse

  94. Department of Pulmonary Medicine, University of Turku and Turku University Hospital, Turku, Finland

    Tarja Laitinen

  95. Département des Sciences Fondamentales, Université du Québec à Chicoutimi, Chicoutimi, Quebec, Canada

    Catherine Laprise

  96. Centre de Santé et de Services Sociaux du Saguenay-Lac-Saint-Jean, Saguenay, QC, Canada

    Catherine Laprise

  97. McGill University and Genome Quebec Innovation Centre, Montréal, QC, Canada

    Mark Lathrop

  98. Pediatric Pneumology and Immunology, Charité Universitätsmedizin, Berlin, Germany

    Susanne Lau

  99. Max-Delbrück-Centrum (MDC) for Molecular Medicine, Berlin, Germany

    Young-Ae Lee & Ingo Marenholz

  100. Pediatric Allergology, Experimental and Clinical Research Center, Charité Universitätsmedizin, Berlin, Germany

    Young-Ae Lee & Ingo Marenholz

  101. Department of Clinical Chemistry, Fimlab Laboratories, Faculty of Medicine and Life Sciences, University of Tampere, Tampere, Finland

    Terho Lehtimäki

  102. Department of Public Health Sciences, Henry Ford Health System, Detroit, MI, USA

    Albert M. Levin

  103. Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Liming Liang

  104. Division of General Medicine, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

    Laura R. Loehr

  105. National Institute of Environmental Health Sciences, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, NC, USA

    Stephanie J. London

  106. Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA

    Ani Manichaikul & Stephen S. Rich

  107. Melbourne School of Population and Global Health, University of Melbourne, Melbourne, Victoria, Australia

    Melanie C. Matheson

  108. Division of Allergy & Clinical Immunology, Department of Medicine, Johns Hopkins University, Baltimore, MD, USA

    Rasika A. Mathias

  109. Department of Allergy and Clinical Immunology, National Research Institute for Child Health and Development, Tokyo, Japan

    Kenji Matsumoto

  110. Bristol Bioresource Laboratories, School of Social and Community Medicine, University of Bristol, Bristol, UK

    Wendy L. McArdle

  111. Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

    Mads Melbye

  112. Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA

    Mads Melbye

  113. Centre for Occupational and Environmental Medicine, Stockholm County Council, Stockholm, Sweden

    Erik Melén & Göran Pershagen

  114. Sachs Children’s Hospital, Stockholm, Sweden

    Erik Melén

  115. Department of Respiratory Medicine, Sir Charles Gairdner Hospital, Nedlands, Western Australia, Australia

    Arthur W. Musk

  116. Schools of Population Health and of Medicine and Pharmacology, University of Western Australia, Perth, Western Australia, Australia

    Arthur W. Musk

  117. Center for Applied Genomics and Precision Medicine, Duke University School of Medicine, Durham, NC, USA

    Rachel A. Myers

  118. University Medical Center Groningen, Department of Pulmonology, University of Groningen, Groningen, The Netherlands

    Maartje A. E. Nieuwenhuis & Dirkje S. Postma

  119. Department of Medical Genetics, Faculty of Medicine, University of Tsukuba, Tsukuba, Japan

    Emiko Noguchi

  120. Pulmonary Center, Department of Medicine, Boston University School of Medicine, Boston, MA, USA

    George T. O’Connor

  121. The National Heart, Lung, and Blood Institute’s Framingham Heart Study, Framingham, MA, USA

    George T. O’Connor

  122. Department of Faculty Pediatrics, Siberian State Medical University, Tomsk, Russian Federation

    Ludmila M. Ogorodova

  123. Analytic and Translational Genetics Unit, Departments of Medicine, of Neurology and of Psychiatry, Massachusetts General Hospital, Boston, MA, USA

    Aarno Palotie

  124. The Stanley Center for Psychiatric Research and Program in Medical and Population Genetics, Broad Institute, Cambridge, MA, USA

    Aarno Palotie

  125. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Benjamin A. Raby & Scott T. Weiss

  126. Department of Clinical Physiology and Nuclear Medicine, University of Turku and Turku University Hospital, Turku, Finland

    Olli T. Raitakari

  127. Department of Medical and Molecular Genetics, King’s College London, London, UK

    Adaikalavan Ramasamy

  128. Respiratory Medicine, Murdoch Children’s Research Institute, Melbourne, Victoria, Australia

    Colin F. Robertson

  129. Hubert Department of Global Health, Mory University, Atlanta, GA, USA

    Isabelle Romieu

  130. Center for Population Health Research, National Institute of Public Health, Cuernavaca, Mexico

    Isabelle Romieu

  131. Department of Psychiatry, Kern Medical, Bakersfield, CA, USA

    Muhammad T. Salam

  132. Department of Public Health, Section for Environment, Occupation & Health, Aarhus University, Aarhus, Denmark

    Vivi Schlünssen & Torben Sigsgaard

  133. MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, UK

    Robert Scott, Nick J. Wareham & Jing Hua Zhao

  134. Department of Faculty Therapy, Siberian State Medical University, Tomsk, Russian Federation

    Polina A. Selivanova

  135. University Hospital of South Manchester, National Health Service (NHS) Foundation Trust, Manchester, UK

    Angela Simpson

  136. Institut National de la Santé et de la Recherche Médicale (INSERM) U1209, Institute for Advanced Biosciences, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France

    Valérie Siroux

  137. Université de Grenoble Alpes/CNRS UMR5309, Institute for Advanced Biosciences, Team of Environmental Epidemiology Applied to Reproduction and Respiratory Health, Grenoble, France

    Valérie Siroux

  138. Division of Pulmonary and Critical Care Medicine, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    Lewis J. Smith

  139. Population Health Research Institute, St George’s University of London, London, UK

    David P. Strachan

  140. Netherlands Healthcare Inspectorate, The Hague, The Netherlands

    Bruno H. Stricker

  141. Department of Internal Medicine, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Bruno H. Stricker & André G. Uitterlinden

  142. Institute for Respiratory Health and Harry Perkins Institute of Medical Research, University of Western Australia and The Lung Health Clinic, Nedlands, Western Australia, Australia

    Philip J. Thompson

  143. Division of Metabolic Diseases and Nutritional Medicine, Dr. von Hauner Children’s Hospital, Ludwig-Maximilians-University of Munich, Munich, Germany

    Carla M. T. Tiesler

  144. Department of Medical Science Mathematics, Medical Research Institute, Tokyo Medical and Dental University, Tokyo, Japan

    Tatsuhiko Tsunoda

  145. The Generation R Study Group, Department of Pediatrics, Division of Respiratory Medicine and Department of Epidemiology, Erasmus MC–University Medical Center Rotterdam, Rotterdam, The Netherlands

    Ralf J. P. van der Valk

  146. Department of Pediatrics, Marien-Hospital Wesel, Wesel, Germany

    Andrea von Berg

  147. Dr. Von Hauner Children’s Hospital, Ludwig Maximilians University Munich, Munich, Germany

    Erika von Mutius

  148. German Center for Lung Research, Munich, Germany

    Erika von Mutius

  149. University of Groningen, University Medical Center Groningen, Department of Epidemiology, Groningen, The Netherlands

    Judith M. Vonk

  150. Undergraduate Training and Education Center (UTEC), Jackson Heart Study, Tougaloo College, Jackson, MI, USA

    Wendy B. White

  151. Centre for Clinical Research Sörmland, Uppsala University, Eskilstuna, Sweden

    Magnus Wickman

  152. Center for Health Policy and Health Services Research, Henry Ford Health System, Detroit, MI, USA

    L. Keoki Williams

  153. Department of Internal Medicine, Henry Ford Health System, Detroit, MI, USA

    L. Keoki Williams

  154. School of Nursing, University of Michigan, Ann Arbor, MI, USA

    James J. Yang

  155. Department of Human Genetics, University of Chicago, Chicago, IL, USA

    Carole Ober

  156. Departments of Statistics, Human Genetics and Medicine, Section of Genetic Medicine, University of Chicago, Chicago, IL, USA

    Dan L. Nicolae

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Consortia

Australian Asthma Genetics Consortium (AAGC) collaborators

Contributions

TAGC study management: F.D., K.C.B., W.O.C.C., M.F.M., C.O., and D.L.N.

F.D. and D.L.N. designed the study and wrote the manuscript. F.D., D.L.N., and P.M.-J. designed and conducted the statistical analysis. K.C.B., W.O.C.C., M.F.M., and C.O. designed the study and wrote the manuscript. M.B., A.V., S. Letort, and H.M. carried out the quality control of the data and performed statistical analysis.

AAGC (Australia): study principal investigators (PIs), M.A.F., M.C.M., C.F.R., and P.J.T.; data collection or analysis, M.A.F., M.C.M., C.F.R., G.J., and P.J.T.

ALLERGEN Canadian Asthma Primary Prevention Study (CAPPS) and Study of Asthma, Genes and the Environment (SAGE): study PIs, A.B.B., M.C.-Y., D.D., and A.L.K.; data collection or analysis, D.D. and J.E.P.; study phenotyping, A.B.B. and M.C.-Y.

Saguenay‐Lac‐Saint‐Jean (SLSJ) Study: study PIs, C.L. and T.J.H.; study design and management, C.L.

Analysis in Population-based Cohorts of Asthma Traits (APCAT) Consortium: study PIs, J.N.H., M.-R.J., and V. Salomaa. Framingham Heart Study (FHS): study PI, G.T.O.; data collection or analysis, S.V. and Z.G. The European Prospective Investigation of Cancer (EPIC)-Norfolk: study PI, N.J.W.; data collection or analysis, J.H.Z. and R.S. Northern Finland Birth Cohort of 1966 (NFBC1966): study PI, M.-R.J.; data collection or analysis, A.C.A. and A.R. FINRISK: study PI, V. Salomaa; data collection or analysis, M. Kuokkanen and T. Laitinen. Health 2000 (H2000) Survey: study PIs, M.H. and P.J.; data collection or analysis, M. Kuokkanen and T.H. Helsinki Birth Cohort Study (HBCS): study PI, J.G.E.; data collection or analysis, E.W. and A. Palotie. Young Finns Study (YFS): study PI, O.T.R.; data collection or analysis, T. Lehtimäki and M. Kähönen.

African Ancestry Studies from the Candidate Gene Association Resource (CARe) Consortium: study PIs, J.N.H. and S.S.R.; data collection or analysis, C.D.P., D.B.K., L.J.S., R.K., K.M.B., and W.B.W.

Multi‐Ethnic Study of Atherosclerosis (MESA): study PIs, R.G.B. and S.S.R.; data collection or analysis, K.M.D. and A.M.

Atherosclerosis Risk in Communities Study (ARIC): study PI, S.J.L.; data collection or analysis, S.J.L. and L.R.L.

Cardiovascular Health Study (CHS): study PIs, S.A.G. and S.R.H.; data collection or analysis, G.L., S.A.G., and S.R.H.

deCode genetics: study PIs, K.S., I.J., D.F.G., U.T., and G.T.; data collection or analysis, I.J., D.F.G., and G.T.; study phenotyping, U.S.B.

Early Genetics and Lifecourse Epidemiology (EAGLE) Consortium: PI, H.B. Cophenhagen Prospective Study on Asthma in Childhood (COPSAC): study PIs, H.B. and K.B.; data analysis, E. Kreiner and J.W.; study phenotyping, K.B. Danish National Birth Cohort (DNBC): study PI, M.M.; data collection or analysis, B.F. and F. Geller. GENERATION R: study PI, J.C.d.J.; data collection or analysis, R.J.P.v.d.V., L.D., and V.W.V.J. GINIplus/LISAplus: study PI, J. Heinrich; genotyping, data collection or analysis, M. Standl and C.M.T.T.; study phenotyping, J. Heinrich. Manchester Asthma and Allergy Study (MAAS): study PIs, A.S. and A.C.; data collection or analysis, J.A.C. Western Australian Pregnancy Cohort Study (RAINE): study PI, P.H.; data collection or analysis, W.A. and C.E.P.

British 1958 Birth Cohort (B58C) Study: PI and statistical analysis, D.P.S.

EVE Consortium: study PIs, C.O., D.L.N., K.C.B., E. Bleecker, E. Burchard, J. Gauderman, F. Gilliland, S.J.L., F.J.M., D.M., I.R., S.T.W., L.K.W., and B.A.R.; data collection or analysis, D.L.N., J. Gauderman, S.J.L., D.M., D.G.T., B.A.R., B.E.H., P.E.G., M.T.S., C.E., B.E.D.-R.-N., J.J.Y., A.M.L., R.A. Myers, R.A. Mathias, and T.H.B.

Japanese Adult Asthma Research Consortium (JAARC): study PI, T.T.; data collection or analysis, T.T., A.T., and M. Kubo.

Japan Pediatric Asthma Consortium (JPAC): study PI, E.N.; data collection or analysis, H.H. and K.M.

GABRIEL Consortium: study PIs, W.O.C.C. and E.V.M.; genotyping, M.L.; data analysis, E.B., F.D., M.F., and D.P.S. Epidemiological study on the Genetics and Environment of Asthma (EGEA): study PIs, V. Siroux and F.D.; genotyping, data collection or analysis, M.L. and E. Bouzigon. Avon Longitudinal Study of Parents and Children (ALSPAC): study PI, J. Henderson; genotyping, data collection or analysis, W.L.M. and R.G.; study phenotyping, J. Henderson. European Community Respiratory Health Survey (ECRHS): study PI, D.J.; data collection or analysis, C.J. and J. Heinrich. Children, Allergy, Milieu, Stockholm, Epidemiology (BAMSE) study: study PIs, E.M., M.W., and G.P. Busselton Health Study: study PIs, A.W.M., A.J., and J.B.; genotyping, data collection or analysis, A.W.M., A.J., J. Hui, and J.B. GABRIEL Advanced Surveys: study PI, E.V.M.; data collection or analysis, M. Kabesch and J. Genuneit. Kursk State Medical University (KSMU) Study: study PI, A. Polonikov; data collection or analysis, M. Solodilova and V.I.; Medical Research Council-funded Collection of Nuclear Families with Asthma (MRCA-UKC): study PIs, W.O.C.C. and M.M.; data collection or analysis, L. Liang. Multicentre Asthma Genetics in Childhood Study (MAGICS): study PI, M. Kabesch; data collection or analysis, A.V.B. and S.M. German Multicentre Allergy Study (MAS): study PI, Y.-A.L.; data collection or analysis, S. Lau and I.M. Prevention and Incidence of Asthma and Mite Allergy (PIAMA) cohort : study PIs, G.H.K. and D.S.P.; data collection or analysis, G.H.K., D.S.P., and U.G. Swiss Cohort Study on Air Pollution and Lung and Heart Diseases in Adults (SAPALDIA): study PI, N.P.-H.; data collection or analysis, M.I. and A.K. Tomsk Study: study PIs, L.M.O. and V.P.P.; data collection or analysis, M.B.F. and P.A.S. UFA Study: study PI, E. Khusnutdinova; data collection or analysis, A.S.K. and Y.F. Industrial Cohorts Research Group (INDUSTRIAL): study PIs, D.H. and T.S.; data collection or analysis, I.M.W. and V. Schlünssen. Severe Asthma Cohorts (SEVERE): study PIs, A.B., K.F.C., and C.E.B.

Netherlands Twin Register (NTR) Study: study PI, D.I.B.; genotyping, data collection or analysis, J.J.H., H.M., and G.W.

Rotterdam Study: study PIs, A.H., B.H.S., and G.G.B.; genotyping, data collection or analysis, G.G.B., B.H.S., D.W.L., L. Lahousse, and A.G.U.

Dutch Asthma Genetics Consortium (DAGC): study PIs, G.H.K. and D.S.P.; genotyping, data collection or analysis, G.H.K., D.S.P., J.A., M.A.E.N., and J.M.V.

All authors provided critical review of the manuscript.

Corresponding authors

Correspondence to Florence Demenais or Dan L. Nicolae.

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Competing interests

The authors affiliated with deCODE (D.F.G., I.J., K.S., U.T., and G.T.) are employees of deCODE genetics/Amgen. All other coauthors have no conflicts of interest to declare.

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Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7, Supplementary Tables 3, 5–7, 9, 10, 12–17, 20 and 21, and Supplementary Note.

Life Sciences Reporting Summary

Supplementary Table 1

Description of TAGC studies included in the meta-analysis.

Supplementary Table 2

Information on genotyping methods, imputation, and statistical analysis by study. Details and references for each study are in the Supplementary Note.

Supplementary Table 4

Genome-wide significant SNPs (Prandom ≤ 5 × 10−8) in the European-ancestry meta-analysis.

Supplementary Table 8

Genome-wide significant SNPs (Prandom ≤ 5 × 10−8) in the multi-ancestry meta-analysis.

Supplementary Table 11

Association of 17q12-21 SNPs with asthma in multi-ancestry and pediatric meta-analyses.

Supplementary Table 18

Overlap between TAGC asthma-association signals (Prandom <10−3) and GWAS signals with diseases/traits in the GWAS catalog.

Supplementary Table 19

Enrichment of asthma risk loci in promoter and enhancer marks by cell type. The results presented in this table are for 16 out of the 18 asthma loci shown in Table 1. The 6p21.33 and 6p21.32 loci spanning the HLA complex were excluded because of high variability and LD in the region. Enhancer and promoter marks were defined using the ChromHMM 15-state model applied to 127 ROADMAP/ENCODE reference epigenomes (PMID 25693563).

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Demenais, F., Margaritte-Jeannin, P., Barnes, K.C. et al. Multiancestry association study identifies new asthma risk loci that colocalize with immune-cell enhancer marks. Nat Genet 50, 42–53 (2018). https://doi.org/10.1038/s41588-017-0014-7

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