Genetic fine-mapping and genomic annotation defines causal mechanisms at type 2 diabetes susceptibility loci View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2015-11-09

AUTHORS

Kyle J Gaulton, Teresa Ferreira, Yeji Lee, Anne Raimondo, Reedik Mägi, Michael E Reschen, Anubha Mahajan, Adam Locke, N William Rayner, Neil Robertson, Robert A Scott, Inga Prokopenko, Laura J Scott, Todd Green, Thomas Sparso, Dorothee Thuillier, Loic Yengo, Harald Grallert, Simone Wahl, Mattias Frånberg, Rona J Strawbridge, Hans Kestler, Himanshu Chheda, Lewin Eisele, Stefan Gustafsson, Valgerdur Steinthorsdottir, Gudmar Thorleifsson, Lu Qi, Lennart C Karssen, Elisabeth M van Leeuwen, Sara M Willems, Man Li, Han Chen, Christian Fuchsberger, Phoenix Kwan, Clement Ma, Michael Linderman, Yingchang Lu, Soren K Thomsen, Jana K Rundle, Nicola L Beer, Martijn van de Bunt, Anil Chalisey, Hyun Min Kang, Benjamin F Voight, Gonçalo R Abecasis, Peter Almgren, Damiano Baldassarre, Beverley Balkau, Rafn Benediktsson, Matthias Blüher, Heiner Boeing, Lori L Bonnycastle, Erwin P Bottinger, Noël P Burtt, Jason Carey, Guillaume Charpentier, Peter S Chines, Marilyn C Cornelis, David J Couper, Andrew T Crenshaw, Rob M van Dam, Alex S F Doney, Mozhgan Dorkhan, Sarah Edkins, Johan G Eriksson, Tonu Esko, Elodie Eury, João Fadista, Jason Flannick, Pierre Fontanillas, Caroline Fox, Paul W Franks, Karl Gertow, Christian Gieger, Bruna Gigante, Omri Gottesman, George B Grant, Niels Grarup, Christopher J Groves, Maija Hassinen, Christian T Have, Christian Herder, Oddgeir L Holmen, Astradur B Hreidarsson, Steve E Humphries, David J Hunter, Anne U Jackson, Anna Jonsson, Marit E Jørgensen, Torben Jørgensen, Wen-Hong L Kao, Nicola D Kerrison, Leena Kinnunen, Norman Klopp, Augustine Kong, Peter Kovacs, Peter Kraft, Jasmina Kravic, Cordelia Langford, Karin Leander, Liming Liang, Peter Lichtner, Cecilia M Lindgren, Eero Lindholm, Allan Linneberg, Ching-Ti Liu, Stéphane Lobbens, Jian'an Luan, Valeriya Lyssenko, Satu Männistö, Olga McLeod, Julia Meyer, Evelin Mihailov, Ghazala Mirza, Thomas W Mühleisen, Martina Müller-Nurasyid, Carmen Navarro, Markus M Nöthen, Nikolay N Oskolkov, Katharine R Owen, Domenico Palli, Sonali Pechlivanis, Leena Peltonen, John R B Perry, Carl G P Platou, Michael Roden, Douglas Ruderfer, Denis Rybin, Yvonne T van der Schouw, Bengt Sennblad, Gunnar Sigurðsson, Alena Stančáková, Gerald Steinbach, Petter Storm, Konstantin Strauch, Heather M Stringham, Qi Sun, Barbara Thorand, Emmi Tikkanen, Anke Tonjes, Joseph Trakalo, Elena Tremoli, Tiinamaija Tuomi, Roman Wennauer, Steven Wiltshire, Andrew R Wood, Eleftheria Zeggini, Ian Dunham, Ewan Birney, Lorenzo Pasquali, Jorge Ferrer, Ruth J F Loos, Josée Dupuis, Jose C Florez, Eric Boerwinkle, James S Pankow, Cornelia van Duijn, Eric Sijbrands, James B Meigs, Frank B Hu, Unnur Thorsteinsdottir, Kari Stefansson, Timo A Lakka, Rainer Rauramaa, Michael Stumvoll, Nancy L Pedersen, Lars Lind, Sirkka M Keinanen-Kiukaanniemi, Eeva Korpi-Hyövälti, Timo E Saaristo, Juha Saltevo, Johanna Kuusisto, Markku Laakso, Andres Metspalu, Raimund Erbel, Karl-Heinz Jöcke, Susanne Moebus, Samuli Ripatti, Veikko Salomaa, Erik Ingelsson, Bernhard O Boehm, Richard N Bergman, Francis S Collins, Karen L Mohlke, Heikki Koistinen, Jaakko Tuomilehto, Kristian Hveem, Inger Njølstad, Panagiotis Deloukas, Peter J Donnelly, Timothy M Frayling, Andrew T Hattersley, Ulf de Faire, Anders Hamsten, Thomas Illig, Annette Peters, Stephane Cauchi, Rob Sladek, Philippe Froguel, Torben Hansen, Oluf Pedersen, Andrew D Morris, Collin N A Palmer, Sekar Kathiresan, Olle Melander, Peter M Nilsson, Leif C Groop, Inês Barroso, Claudia Langenberg, Nicholas J Wareham, Christopher A O'Callaghan, Anna L Gloyn, David Altshuler, Michael Boehnke, Tanya M Teslovich, Mark I McCarthy, Andrew P Morris

ABSTRACT

We performed fine mapping of 39 established type 2 diabetes (T2D) loci in 27,206 cases and 57,574 controls of European ancestry. We identified 49 distinct association signals at these loci, including five mapping in or near KCNQ1. 'Credible sets' of the variants most likely to drive each distinct signal mapped predominantly to noncoding sequence, implying that association with T2D is mediated through gene regulation. Credible set variants were enriched for overlap with FOXA2 chromatin immunoprecipitation binding sites in human islet and liver cells, including at MTNR1B, where fine mapping implicated rs10830963 as driving T2D association. We confirmed that the T2D risk allele for this SNP increases FOXA2-bound enhancer activity in islet- and liver-derived cells. We observed allele-specific differences in NEUROD1 binding in islet-derived cells, consistent with evidence that the T2D risk allele increases islet MTNR1B expression. Our study demonstrates how integration of genetic and genomic information can define molecular mechanisms through which variants underlying association signals exert their effects on disease. More... »

PAGES

1415-1425

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  • Journal

    TITLE

    Nature Genetics

    ISSUE

    12

    VOLUME

    47

    Author Affiliations

  • Department of Genetics, Stanford University, Stanford, California, USA.
  • Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK.
  • Department of Biostatistics, University of Michigan, Ann Arbor, Michigan, USA.
  • Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, Oxford, UK.
  • Estonian Genome Center, University of Tartu, Tartu, Estonia.
  • Centre for Cellular and Molecular Physiology, Nuffield Department of Medicine, University of Oxford, Oxford, UK.
  • Wellcome Trust Sanger Institute, Hinxton, UK.
  • Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge, UK.
  • Genomics of Common Disease, Imperial College London, London, UK.
  • Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA.
  • Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
  • Lille Institute of Biology, European Genomics Institute of Diabetes, Lille, France.
  • German Center for Diabetes Research, Neuherberg, Germany.
  • Department for Numerical Analysis and Computer Science, Stockholm University, Stockholm, Sweden.
  • Atherosclerosis Research Unit, Department of Medicine Solna, Karolinska Institutet, Stockholm, Sweden.
  • Medical Systems Biology, Ulm University, Ulm, Germany.
  • Finnish Institute for Molecular Medicine (FIMM), Helsinki, Finland.
  • Institute for Medical Informatics, Biometry and Epidemiology, University Hospital of Essen, Essen, Germany.
  • Department of Medical Sciences, Molecular Epidemiology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.
  • deCODE Genetics/Amgen, Inc., Reykjavik, Iceland.
  • Department of Epidemiology, School of Public Health and Tropical Medicine, Tulane University, New Orleans, Louisiana, USA.
  • Department of Epidemiology, Erasmus University Medical Center, Rotterdam, the Netherlands.
  • Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA.
  • Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, USA.
  • Icahn Institute for Genomics and Multiscale Biology, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
  • Genetics of Obesity and Related Metabolic Traits Program, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
  • Department of Pharmacology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.
  • Lund University Diabetes Centre, Department of Clinical Science Malmo, Scania University Hospital, Lund University, Malmo, Sweden.
  • Dipartimento di Scienze Farmacologiche e Biomolecolari, Università di Milano, Milan, Italy.
  • University Paris Sud 11, UMRS 1018, Villejuif, France.
  • Landspitali University Hospital, Reykjavik, Iceland.
  • Department of Medicine, University of Leipzig, Leipzig, Germany.
  • German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany.
  • National Human Genome Research Institute, US National Institutes of Health, Bethesda, Maryland, USA.
  • Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
  • Endocrinology-Diabetology Unit, Corbeil-Essonnes Hospital, Corbeil-Essonnes, France.
  • Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
  • Collaborative Studies Coordinating Center, Department of Biostatistics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
  • Saw Swee Hock School of Public Health, National University of Singapore, Singapore.
  • Pharmacogenomics Centre, Biomedical Research Institute, University of Dundee, Ninewells Hospital, Dundee, UK.
  • Lund University Diabetes Centre, Department of Clinical Science Malmo, Novo Nordisk Scandinavia, Malmo, Sweden.
  • Folkhalsan Research Center, Helsinki, Finland.
  • Program in Medical and Population Genetics, Broad Institute of Harvard and MIT, Cambridge, Massachusetts, USA.
  • CNRS UMR 8199, Institute of Biology and Lille 2 University, Pasteur Institute, Lille, France.
  • Division of Endocrinology and Metabolism, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
  • Department of Public Health and Clinical Medicine, Umea University, Umea, Sweden.
  • Institute of Epidemiology II, Helmholtz Zentrum München-German Research Center for Environmental Health, Neuherberg, Germany.
  • Division of Cardiovascular Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden.
  • Kuopio Research Institute of Exercise Medicine, Kuopio, Finland.
  • German Center for Diabetes Research, partner site Dusseldorf, Dusseldorf, Germany.
  • Nord-Trøndelag Health Study (HUNT) Research Center, Department of Public Health and General Practice, Norwegian University of Science and Technology, Levanger, Norway.
  • Cardiovascular Genetics, British Heart Foundation (BHF) Laboratories, Institute of Cardiovascular Sciences, University College London, London, UK.
  • Program in Genetic Epidemiology and Statistical Genetics, Harvard School of Public Health, Boston, Massachusetts, USA.
  • Steno Diabetes Center, Gentofte, Denmark.
  • Faculty of Medicine, University of Aalborg, Aalborg, Denmark.
  • Department of Chronic Disease Prevention, National Institute for Health and Welfare, Helsinki, Finland.
  • Hannover Unified Biobank, Hannover Medical School, Hannover, Germany.
  • Institute of Human Genetics, Helmholtz Zentrum München-German Research Center for Environmental Health, Neuherberg, Germany.
  • Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark.
  • Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts, USA.
  • Institute of Genetic Epidemiology, Helmholtz Zentrum München-German Research Center for Environmental Health, Neuherberg, Germany.
  • Biomedical Research Centre Genomics Core Facility, Guy's and St Thomas' National Health Service (NHS) Foundation Trust, Guy's &St Thomas' Hospital, London, UK.
  • Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich, Jülich, Germany.
  • DZHK (German Center for Cardiovascular Research), partner site Munich Heart Alliance, Munich, Germany.
  • Department of Health and Social Sciences, Universidad de Murcia, Murcia, Spain.
  • Department of Genomics, Life and Brain Center, University of Bonn, Bonn, Germany.
  • Oxford National Institute for Health Research Biomedical Research Centre, Churchill Hospital, Oxford, UK.
  • Cancer Research and Prevention Institute (ISPO), Florence, Italy.
  • Department of Internal Medicine, Levanger Hospital, Nord-Trondelag Health Trust, Levanger, Norway.
  • Department of Endocrinology and Diabetology, University Hospital Dusseldorf, Dusseldorf, Germany.
  • Division of Psychiatric Genomics, Department of Psychiatry, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
  • Boston University Data Coordinating Center, Boston, Massachusetts, USA.
  • University Medical Center Utrecht, Utrecht, the Netherlands.
  • Science for Life Laboratory, Stockholm, Sweden.
  • Icelandic Heart Association, Kopavogur, Iceland.
  • Department of Medicine, University of Eastern Finland and Kuopio University Hospital, Kuopio, Finland.
  • Department of Clinical Chemistry and Central Laboratory, University of Ulm, Ulm, Germany.
  • Institute of Medical Informatics, Biometry and Epidemiology, Chair of Genetic Epidemiology, Ludwig Maximilians Universität, Neuherberg, Germany.
  • Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts, USA.
  • Department of Public Health, Hjelt Institute, University of Helsinki, Helsinki, Finland.
  • Research Program for Diabetes and Obesity, University of Helsinki, Helsinki, Finland.
  • Department of Internal Medicine, Erasmus University Medical Center, Rotterdam, the Netherlands.
  • Genetics of Complex Traits, University of Exeter Medical School, University of Exeter, Exeter, UK.
  • European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Hinxton, UK.
  • CIBER de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Barcelona, Spain.
  • Institut d'Investigacions Biomèdiques August Pi i Sunyer, Centre Esther Koplowitz, Barcelona, Spain.
  • Mindich Child Health and Development Institute, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
  • National Heart, Lung, and Blood Institute's Framingham Heart Study, Framingham, Massachusetts, USA.
  • Diabetes Research Center, Diabetes Unit, Massachusetts General Hospital, Boston, Massachusetts, USA.
  • Human Genome Sequencing Center at Baylor College of Medicine, Houston, Texas, USA.
  • Division of Epidemiology and Community Health, University of Minnesota, Minneapolis, Minnesota, USA.
  • Netherlands Genomics Initiative, Netherlands Consortium for Healthy Ageing and Center for Medical Systems Biology, Rotterdam, the Netherlands.
  • General Medicine Division, Massachusetts General Hospital, Boston, Massachusetts, USA.
  • Faculty of Medicine, University of Iceland, Reykjavik, Iceland.
  • Department of Clinical Physiology and Nuclear Medicine, Kuopio University Hospital, Kuopio, Finland.
  • Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
  • Department of Medical Sciences, Uppsala University Hospital, Uppsala, Sweden.
  • Unit of General Practice, Oulu University Hospital, Oulu, Finland.
  • South Ostrobothnia Central Hospital, Seinajoki, Finland.
  • Pirkanmaa District Hospital, Tampere, Finland.
  • Department of Medicine, Central Finland Central Hospital, Jyvasklya, Finland.
  • Institute of Molecular and Cell Biology, University of Tartu, Tartu, Estonia.
  • Clinic of Cardiology, West German Heart Centre, University Hospital of Essen, University Duisdurg-Essen, Essen, Germany.
  • Institute of Biomedicine/Physiology, University of Eastern Finland, Kuopio, Finland.
  • Public Health Genomics Unit, National Institute for Health and Welfare, Helsinki, Finland.
  • Lee Kong Chian School of Medicine, Imperial College London and Nanyang Technological University, Singapore.
  • Diabetes and Obesity Research Institute, Cedars-Sinai Medical Center, Los Angeles, California, USA.
  • Department of Genetics, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA.
  • Minerva Foundation Institute for Medical Research, Helsinki, Finland.
  • Diabetes Research Group, King Abdulaziz University, Jeddah, Saudi Arabia.
  • Department of Community Medicine, Faculty of Health Sciences, University of Tromso, Tromso, Norway.
  • William Harvey Research Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, UK.
  • Department of Statistics, University of Oxford, Oxford, UK.
  • Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, UK.
  • McGill University and Génome Québec Innovation Centre, Montreal, Quebec, Canada.
  • Faculty of Health Sciences, University of Southern Denmark, Odense, Denmark.
  • Usher Institute of Population Health Sciences and Informatics, University of Edinburgh, Edinburgh, UK.
  • Cardiovascular Research Center, Massachusetts General Hospital, Boston, Massachusetts, USA.
  • National Institute for Health Research Cambridge Biomedical Research Centre, Cambridge, UK.
  • Department of Molecular Biology, Harvard Medical School, Boston, Massachusetts, USA.
  • Department of Molecular and Clinical Pharmacology, University of Liverpool, Liverpool, UK.
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/ng.3437

    DOI

    http://dx.doi.org/10.1038/ng.3437

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1041209717

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/26551672


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