Rare and low-frequency coding variants alter human adult height View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2017-02-01

AUTHORS

Eirini Marouli, Mariaelisa Graff, Carolina Medina-Gomez, Ken Sin Lo, Andrew R. Wood, Troels R. Kjaer, Rebecca S. Fine, Yingchang Lu, Claudia Schurmann, Heather M. Highland, Sina Rüeger, Gudmar Thorleifsson, Anne E. Justice, David Lamparter, Kathleen E. Stirrups, Valérie Turcot, Kristin L. Young, Thomas W. Winkler, Tõnu Esko, Tugce Karaderi, Adam E. Locke, Nicholas G. D. Masca, Maggie C. Y. Ng, Poorva Mudgal, Manuel A. Rivas, Sailaja Vedantam, Anubha Mahajan, Xiuqing Guo, Goncalo Abecasis, Katja K. Aben, Linda S. Adair, Dewan S. Alam, Eva Albrecht, Kristine H. Allin, Matthew Allison, Philippe Amouyel, Emil V. Appel, Dominique Arveiler, Folkert W. Asselbergs, Paul L. Auer, Beverley Balkau, Bernhard Banas, Lia E. Bang, Marianne Benn, Sven Bergmann, Lawrence F. Bielak, Matthias Blüher, Heiner Boeing, Eric Boerwinkle, Carsten A. Böger, Lori L. Bonnycastle, Jette Bork-Jensen, Michiel L. Bots, Erwin P. Bottinger, Donald W. Bowden, Ivan Brandslund, Gerome Breen, Murray H. Brilliant, Linda Broer, Amber A. Burt, Adam S. Butterworth, David J. Carey, Mark J. Caulfield, John C. Chambers, Daniel I. Chasman, Yii-Der Ida Chen, Rajiv Chowdhury, Cramer Christensen, Audrey Y. Chu, Massimiliano Cocca, Francis S. Collins, James P. Cook, Janie Corley, Jordi Corominas Galbany, Amanda J. Cox, Gabriel Cuellar-Partida, John Danesh, Gail Davies, Paul I. W. de Bakker, Gert J. de Borst, Simon de Denus, Mark C. H. de Groot, Renée de Mutsert, Ian J. Deary, George Dedoussis, Ellen W. Demerath, Anneke I. den Hollander, Joe G. Dennis, Emanuele Di Angelantonio, Fotios Drenos, Mengmeng Du, Alison M. Dunning, Douglas F. Easton, Tapani Ebeling, Todd L. Edwards, Patrick T. Ellinor, Paul Elliott, Evangelos Evangelou, Aliki-Eleni Farmaki, Jessica D. Faul, Mary F. Feitosa, Shuang Feng, Ele Ferrannini, Marco M. Ferrario, Jean Ferrieres, Jose C. Florez, Ian Ford, Myriam Fornage, Paul W. Franks, Ruth Frikke-Schmidt, Tessel E. Galesloot, Wei Gan, Ilaria Gandin, Paolo Gasparini, Vilmantas Giedraitis, Ayush Giri, Giorgia Girotto, Scott D. Gordon, Penny Gordon-Larsen, Mathias Gorski, Niels Grarup, Megan L. Grove, Vilmundur Gudnason, Stefan Gustafsson, Torben Hansen, Kathleen Mullan Harris, Tamara B. Harris, Andrew T. Hattersley, Caroline Hayward, Liang He, Iris M. Heid, Kauko Heikkilä, Øyvind Helgeland, Jussi Hernesniemi, Alex W. Hewitt, Lynne J. Hocking, Mette Hollensted, Oddgeir L. Holmen, G. Kees Hovingh, Joanna M. M. Howson, Carel B. Hoyng, Paul L. Huang, Kristian Hveem, M. Arfan Ikram, Erik Ingelsson, Anne U. Jackson, Jan-Håkan Jansson, Gail P. Jarvik, Gorm B. Jensen, Min A. Jhun, Yucheng Jia, Xuejuan Jiang, Stefan Johansson, Marit E. Jørgensen, Torben Jørgensen, Pekka Jousilahti, J. Wouter Jukema, Bratati Kahali, René S. Kahn, Mika Kähönen, Pia R. Kamstrup, Stavroula Kanoni, Jaakko Kaprio, Maria Karaleftheri, Sharon L. R. Kardia, Fredrik Karpe, Frank Kee, Renske Keeman, Lambertus A. Kiemeney, Hidetoshi Kitajima, Kirsten B. Kluivers, Thomas Kocher, Pirjo Komulainen, Jukka Kontto, Jaspal S. Kooner, Charles Kooperberg, Peter Kovacs, Jennifer Kriebel, Helena Kuivaniemi, Sébastien Küry, Johanna Kuusisto, Martina La Bianca, Markku Laakso, Timo A. Lakka, Ethan M. Lange, Leslie A. Lange, Carl D. Langefeld, Claudia Langenberg, Eric B. Larson, I-Te Lee, Terho Lehtimäki, Cora E. Lewis, Huaixing Li, Jin Li, Ruifang Li-Gao, Honghuang Lin, Li-An Lin, Xu Lin, Lars Lind, Jaana Lindström, Allan Linneberg, Yeheng Liu, Yongmei Liu, Artitaya Lophatananon, Jian'an Luan, Steven A. Lubitz, Leo-Pekka Lyytikäinen, David A. Mackey, Pamela A. F. Madden, Alisa K. Manning, Satu Männistö, Gaëlle Marenne, Jonathan Marten, Nicholas G. Martin, Angela L. Mazul, Karina Meidtner, Andres Metspalu, Paul Mitchell, Karen L. Mohlke, Dennis O. Mook-Kanamori, Anna Morgan, Andrew D. Morris, Andrew P. Morris, Martina Müller-Nurasyid, Patricia B. Munroe, Mike A. Nalls, Matthias Nauck, Christopher P. Nelson, Matt Neville, Sune F. Nielsen, Kjell Nikus, Pål R. Njølstad, Børge G. Nordestgaard, Ioanna Ntalla, Jeffrey R. O'Connel, Heikki Oksa, Loes M. Olde Loohuis, Roel A. Ophoff, Katharine R. Owen, Chris J. Packard, Sandosh Padmanabhan, Colin N. A. Palmer, Gerard Pasterkamp, Aniruddh P. Patel, Alison Pattie, Oluf Pedersen, Peggy L. Peissig, Gina M. Peloso, Craig E. Pennell, Markus Perola, James A. Perry, John R. B. Perry, Thomas N. Person, Ailith Pirie, Ozren Polasek, Danielle Posthuma, Olli T. Raitakari, Asif Rasheed, Rainer Rauramaa, Dermot F. Reilly, Alex P. Reiner, Frida Renström, Paul M. Ridker, John D. Rioux, Neil Robertson, Antonietta Robino, Olov Rolandsson, Igor Rudan, Katherine S. Ruth, Danish Saleheen, Veikko Salomaa, Nilesh J. Samani, Kevin Sandow, Yadav Sapkota, Naveed Sattar, Marjanka K. Schmidt, Pamela J. Schreiner, Matthias B. Schulze, Robert A. Scott, Marcelo P. Segura-Lepe, Svati Shah, Xueling Sim, Suthesh Sivapalaratnam, Kerrin S. Small, Albert Vernon Smith, Jennifer A. Smith, Lorraine Southam, Timothy D. Spector, Elizabeth K. Speliotes, John M. Starr, Valgerdur Steinthorsdottir, Heather M. Stringham, Michael Stumvoll, Praveen Surendran, Leen M. ‘t Hart, Katherine E. Tansey, Jean-Claude Tardif, Kent D. Taylor, Alexander Teumer, Deborah J. Thompson, Unnur Thorsteinsdottir, Betina H. Thuesen, Anke Tönjes, Gerard Tromp, Stella Trompet, Emmanouil Tsafantakis, Jaakko Tuomilehto, Anne Tybjaerg-Hansen, Jonathan P. Tyrer, Rudolf Uher, André G. Uitterlinden, Sheila Ulivi, Sander W. van der Laan, Andries R. Van Der Leij, Cornelia M. van Duijn, Natasja M. van Schoor, Jessica van Setten, Anette Varbo, Tibor V. Varga, Rohit Varma, Digna R. Velez Edwards, Sita H. Vermeulen, Henrik Vestergaard, Veronique Vitart, Thomas F. Vogt, Diego Vozzi, Mark Walker, Feijie Wang, Carol A. Wang, Shuai Wang, Yiqin Wang, Nicholas J. Wareham, Helen R. Warren, Jennifer Wessel, Sara M. Willems, James G. Wilson, Daniel R. Witte, Michael O. Woods, Ying Wu, Hanieh Yaghootkar, Jie Yao, Pang Yao, Laura M. Yerges-Armstrong, Robin Young, Eleftheria Zeggini, Xiaowei Zhan, Weihua Zhang, Jing Hua Zhao, Wei Zhao, Wei Zhao, He Zheng, Wei Zhou, Jerome I Rotter, Michael Boehnke, Sekar Kathiresan, Mark I. McCarthy, Cristen J. Willer, Kari Stefansson, Ingrid B. Borecki, Dajiang J. Liu, Kari E. North, Nancy L. Heard-Costa, Tune H. Pers, Cecilia M. Lindgren, Claus Oxvig, Zoltán Kutalik, Fernando Rivadeneira, Ruth J. F. Loos, Timothy M. Frayling, Joel N. Hirschhorn, Panos Deloukas, Guillaume Lettre

ABSTRACT

Height is a highly heritable, classic polygenic trait with approximately 700 common associated variants identified through genome-wide association studies so far. Here, we report 83 height-associated coding variants with lower minor-allele frequencies (in the range of 0.1–4.8%) and effects of up to 2 centimetres per allele (such as those in IHH, STC2, AR and CRISPLD2), greater than ten times the average effect of common variants. In functional follow-up studies, rare height-increasing alleles of STC2 (giving an increase of 1–2 centimetres per allele) compromised proteolytic inhibition of PAPP-A and increased cleavage of IGFBP-4 in vitro, resulting in higher bioavailability of insulin-like growth factors. These 83 height-associated variants overlap genes that are mutated in monogenic growth disorders and highlight new biological candidates (such as ADAMTS3, IL11RA and NOX4) and pathways (such as proteoglycan and glycosaminoglycan synthesis) involved in growth. Our results demonstrate that sufficiently large sample sizes can uncover rare and low-frequency variants of moderate-to-large effect associated with polygenic human phenotypes, and that these variants implicate relevant genes and pathways. More... »

PAGES

186-190

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  • Journal

    TITLE

    Nature

    ISSUE

    7640

    VOLUME

    542

    Author Affiliations

  • William Harvey Research Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, EC1M 6BQ, London, UK
  • Department of Epidemiology, University of North Carolina, 27514, Chapel Hill, North Carolina, USA
  • Department of Internal Medicine, Erasmus Medical Center, 3015 GE, Rotterdam, The Netherlands
  • Montreal Heart Institute, H1T 1C8, Montreal, Quebec, Canada
  • Genetics of Complex Traits, University of Exeter Medical School, University of Exeter, EX2 5DW, Exeter, UK
  • Department of Molecular Biology and Genetics, Aarhus University, 8000, Aarhus, Denmark
  • Division of Endocrinology and Center for Basic and Translational Obesity Research, Boston Children’s Hospital, 02115, Boston, Massachusetts, USA
  • The Genetics of Obesity and Related Metabolic Traits Program, Ichan School of Medicine at Mount Sinai, 10069, New York, New York, USA
  • Human Genetics Center, The University of Texas School of Public Health, The University of Texas Graduate School of Biomedical Sciences at Houston, The University of Texas Health Science Center at Houston, 77030, Houston, Texas, USA
  • Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland
  • deCODE Genetics/Amgen inc., 101, Reykjavik, Iceland
  • Department of Computational Biology, University of Lausanne, 1011, Lausanne, Switzerland
  • Department of Haematology, University of Cambridge, CB2 0PT, Cambridge, UK
  • Department of Genetic Epidemiology, University of Regensburg, D-93051, Regensburg, Germany
  • Estonian Genome Center, University of Tartu, 51010, Tartu, Estonia
  • Wellcome Trust Centre for Human Genetics, University of Oxford, OX3 7BN, Oxford, UK
  • McDonnell Genome Institute, Washington University School of Medicine, 63108, Saint Louis, Missouri, USA
  • NIHR Leicester Cardiovascular Biomedical Research Unit, Glenfield Hospital, LE3 9QP, Leicester, UK
  • Center for Genomics and Personalized Medicine Research, Wake Forest School of Medicine, 27157, Winston-Salem, North Carolina, USA
  • Center for Diabetes Research, Wake Forest School of Medicine, 27157, Winston-Salem, North Carolina, USA
  • Nuffield Department of Clinical Medicine, OX3 7BN, Oxford, UK
  • Institute for Translational Genomics and Population Sciences, LABioMed at Harbor-UCLA Medical Center, 90502, Torrance, California, USA
  • Department of Biostatistics and Center for Statistical Genetics, University of Michigan, 48109, Ann Arbor, Michigan, USA
  • Radboud University Medical Center, 6500 HB, Nijmegen, The Netherlands
  • Department of Nutrition, University of North Carolina, 27599, Chapel Hill, North Carolina, USA
  • Centre for Control of Chronic Diseases (CCCD), 1212, Dhaka, Bangladesh
  • Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, D-85764, Neuherberg, Germany
  • The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2100, Copenhagen, Denmark
  • Department of Family Medicine & Public Health, University of California, San Diego, 92093, La Jolla, California, USA
  • Universite de Lille, U1167 - RID-AGE - Risk factors and molecular determinants of aging-related diseases, F-59019, Lille, France
  • Department of Public Health, University Hospital of Strasbourg, 67081, Strasbourg, France
  • Institute of Cardiovascular Science, Faculty of Population Health Sciences, University College London, London, UK
  • Zilber School of Public Health, University of Wisconsin-Milwaukee, 53201, Milwaukee, Wisconsin, USA
  • INSERM U1018, Centre de recherche en Épidemiologie et Sante des Populations (CESP), Villejuif, France
  • Department of Nephrology, University Hospital Regensburg, 93042, Regensburg, Germany
  • Department of Cardiology, Rigshospitalet, Copenhagen University Hospital, 2100, Copenhagen, Denmark
  • Faculty of Health and Medical Sciences, University of Copenhagen, 2200, Copenhagen, Denmark
  • Department of Epidemiology, School of Public Health, University of Michigan, 48109, Ann Arbor, Michigan, USA
  • Department of Medicine, University of Leipzig, 04103, Leipzig, Germany
  • Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke (DIfE), 14558, Nuthetal, Germany
  • Human Genome Sequencing Center, Baylor College of Medicine, 77030, Houston, Texas, USA
  • Medical Genomics and Metabolic Genetics Branch, National Human Genome Research Institute, National Institutes of Health, 20892, Bethesda, Maryland, USA
  • Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands
  • The Charles Bronfman Institute for Personalized Medicine, Icahn School of Medicine at Mount Sinai, 10029, New York, New York, USA
  • Department of Biochemistry, Wake Forest School of Medicine, 27157, Winston-Salem, North Carolina, USA
  • Institute of Regional Health Research, University of Southern Denmark, 5000, Odense, Denmark
  • MRC Social Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology and Neuroscience, King’s College London & NIHR Biomedical Research Centre for Mental Health at the Maudsley, SE5 8AF, London, UK
  • Marshfield Clinic Research Foundation, 54449, Marshfield, Wisconsin, USA
  • Department of Medicine, University of Washington, 98195, Seattle, Washington, USA
  • NIHR Blood and Transplant Research Unit in Donor Health and Genomics, University of Cambridge, CB1 8RN, Cambridge, UK
  • The Sigfried and Janet Weis Center for Research, 17822, Danville, Pennsylvania, USA
  • NIHR Barts Cardiovascular Research Unit, Barts and The London School of Medicine & Dentistry, Queen Mary University, EC1M 6BQ, London, UK
  • Imperial College Healthcare NHS Trust, W12 0HS, London, UK
  • Harvard Medical School, 02115, Boston, Massachusetts, USA
  • Department of Public Health and Primary Care, MRC/BHF Cardiovascular Epidemiology Unit, University of Cambridge, CB1 8RN, Cambridge, UK
  • Medical Department, Lillebaelt Hospital, 7100, Vejle, Denmark
  • NHLBI Framingham Heart Study, 01702, Framingham, Massachusetts, USA
  • Department of Medical, Surgical and Health Sciences, University of Trieste, 34100, Trieste, Italy
  • Department of Biostatistics, University of Liverpool, L69 3GL, Liverpool, UK
  • Department of Psychology, University of Edinburgh, EH8 9JZ, Edinburgh, UK
  • Department of Human Genetics, Radboud University Medical Center, 6500 HB, Nijmegen, The Netherlands
  • Menzies Health Institute Queensland, Griffith University, Southport, Queensland, Australia
  • QIMR Berghofer Medical Research Institute, 4006, Brisbane, Queensland, Australia
  • Department of Medicine, British Heart Foundation, Cambridge Centre of Excellence, University of Cambridge, CB2 0QQ, Cambridge, UK
  • Department of Genetics, Center for Molecular Medicine, University Medical Center Utrecht, 3584 CX, Utrecht, The Netherlands
  • Department of Vascular Surgery, Division of Surgical Specialties, University Medical Center Utrecht, 3584 CX, Utrecht, The Netherlands
  • Faculty of Pharmacy, Université de Montréal, H3T 1J4, Montreal, Quebec, Canada
  • Division Pharmacoepidemiology & Clinical Pharmacology, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, 3508 TB, Utrecht, The Netherlands
  • Department of Clinical Epidemiology, Leiden University Medical Center, 2300 RC, Leiden, The Netherlands
  • Department of Nutrition and Dietetics, School of Health Science and Education, Harokopio University, 17671, Athens, Greece
  • Division of Epidemiology & Community Health, School of Public Health, University of Minnesota, 55454, Minneapolis, Minnesota, USA
  • Department of Ophthalmology, Radboud University Medical Center, 6500 HB, Nijmegen, The Netherlands
  • Department of Public Health and Primary Care, Centre for Cancer Genetic Epidemiology, University of Cambridge, CB1 8RN, Cambridge, UK
  • MRC Integrative Epidemiology Unit, School of Social & Community Medicine, University of Bristol, BS8 2BN, Bristol, UK
  • Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, 10017, New York, New York, USA
  • Department of Oncology, Centre for Cancer Genetic Epidemiology, University of Cambridge, CB1 8RN, Cambridge, UK
  • Research Unit of Internal Medicine, University of Oulu, FI-90014, Oulu, Finland
  • Division of Epidemiology, Department of Medicine, Institute for Medicine and Public Health, Vanderbilt Genetics Institute, Vanderbilt University, 37203, Nashville, Tennessee, USA
  • Medical and Population Genetics Program, Broad Institute, 02141, Cambridge, Massachusetts, USA
  • Department of Epidemiology and Biostatistics, MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London, W2 1PG, London, UK
  • Department of Hygiene and Epidemiology, University of Ioannina Medical School, 45110, Ioannina, Greece
  • Survey Research Center, Institute for Social Research, University of Michigan, 48104, Ann Arbor, Michigan, USA
  • Division of Statistical Genomics, Department of Genetics, Washington University School of Medicine, 63108, StLouis, Missouri, USA
  • Department of Clinical & Experimental Medicine, University of Pisa, Pisa, Italy
  • Department of Clinical and Experimental Medicine, Research Center on Epidemiology and Preventive Medicine, University of Insubria, 21100, Varese, Italy
  • Toulouse University School of Medicine, 50032 31059, Toulouse, TSA, France
  • Department of Medicine, Harvard University Medical School, 02115, Boston, Massachusetts, USA
  • University of Glasgow, G12 8QQ, Glasgow, UK
  • Institute of Molecular Medicine, The University of Texas Health Science Center at Houston, 77030, Houston, Texas, USA
  • Department of Public Health and Clinical Medicine, Unit of Medicine, Umeå University, 901 87, Umeå, Sweden
  • Department of Clinical Biochemistry, Rigshospitalet, Copenhagen University Hospital, 2100, Copenhagen, Denmark
  • Department of Medical Sciences, University of Trieste, 34137, Trieste, Italy
  • Division of Experimental Genetics, Sidra Medical and Research Center, 26999, Doha, Qatar
  • Department of Public Health, Geriatrics, Uppsala University, 751 85, Uppsala, Sweden
  • Department of Nutrition, Gillings School of Global Public Health, University of North Carolina, 27514, Chapel Hill, North Carolina, USA
  • School of Public Health, Human Genetics Center, The University of Texas Health Science Center at Houston, 77030, Houston, Texas, USA
  • Icelandic Heart Association, 201, Kopavogur, Iceland
  • Department of Medical Sciences, Molecular Epidemiology and Science for Life Laboratory, Uppsala University, 751 41, Uppsala, Sweden
  • Department of Sociology, University of North Carolina, 27514, Chapel Hill, North Carolina, USA
  • Laboratory of Epidemiology and Population Sciences, National Institute on Aging, Intramural Research Program, National Institutes of Health, 20892, Bethesda, Maryland, USA
  • University of Exeter Medical School, University of Exeter, EX2 5DW, Exeter, UK
  • MRCHGU, Institute of Genetics and Molecular Medicine, University of Edinburgh, EH4 2XU, Edinburgh, UK
  • Department of Public Health, University of Helsinki, FI-00014, Helsinki, Finland
  • Institute for Molecular Medicine Finland (FIMM), University of Helsinki, FI-00014, Helsinki, Finland
  • Department of Clinical Science, KG Jebsen Center for Diabetes Research, University of Bergen, 5020, Bergen, Norway
  • Department of Clinical Chemistry, University of Tampere School of Medicine, 33014, Tampere, Finland
  • Menzies Research Institute Tasmania, University of Tasmania, 7000, Hobart, Tasmania, Australia
  • Division of Applied Medicine, Musculoskeletal Research Programme, University of Aberdeen, AB25 2ZD, Aberdeen, UK
  • Department of Public Health, K.G. Jebsen Center for Genetic Epidemiology, NTNU, Norwegian University of Science and Technology, 7600, Trondheim, Norway
  • Department of Vascular Medicine, AMC, 1105 AZ, Amsterdam, The Netherlands
  • Massachusetts General Hospital, 02114, Boston, Massachusetts, USA
  • Department of Public Health and General Practice, HUNT Research Centre, Norwegian University of Science and Technology, 7600, Levanger, Norway
  • Department of Radiology, Erasmus Medical Center, 3015 GE, Rotterdam, The Netherlands
  • Department of Medicine, Division of Cardiovascular Medicine, Stanford University School of Medicine, 94305, Stanford, California, USA
  • Research Unit Skellefteå, SE-93141, Skellefteå, Sweden
  • Department of Genome Sciences, University of Washington, 98195, Seattle, Washington, USA
  • The Copenhagen City Heart Study, Frederiksberg Hospital, 2000, Frederiksberg, Denmark
  • Department of Ophthalmology, USC Roski Eye Institute, Keck School of Medicine of the University of Southern California, 90089, Los Angeles, California, USA
  • Center for Medical Genetics and Molecular Medicine, Haukeland University Hospital, 5021, Bergen, Norway
  • Steno Diabetes Center, 2820, Gentofte, Denmark
  • Research Center for Prevention and Health, Capital Region of Denmark, DK-2600, Glostrup, Denmark
  • National Institute for Health and Welfare, FI-00271, Helsinki, Finland
  • The Interuniversity Cardiology Institute of the Netherlands, 2333, Utrecht, The Netherlands
  • Division of Gastroenterology, University of Michigan, 48109, Ann Arbor, Michigan, USA
  • Department of Psychiatry, Brain Center Rudolf Magnus, University Medical Center Utrecht, 3584 CG, Utrecht, The Netherlands
  • Department of Clinical Physiology, University of Tampere School of Medicine, 33014, Tampere, Finland
  • Department of Clinical Biochemistry, Herlev and Gentofte Hospital, Copenhagen University Hospital, 2730, Herlev, Denmark
  • Echinos Medical Centre, Echinos, Greece
  • Oxford NIHR Biomedical Research Centre, Oxford University Hospitals Trust, OX3 7LE, Oxford, UK
  • UKCRC Centre of Excellence for Public Health Research, Queens University Belfast, BT12 6BJ, Belfast, UK
  • Netherlands Cancer Institute - Antoni van Leeuwenhoek hospital, 1066 CX, Amsterdam, The Netherlands
  • Department of Restorative Dentistry, Periodontology and Endodontology, University Medicine Greifswald, 17475, Greifswald, Germany
  • Foundation for Research in Health Exercise and Nutrition, Kuopio Research Institute of Exercise Medicine, 70100, Kuopio, Finland
  • National Heart and Lung Institute, Imperial College London, Hammersmith Hospital Campus, W12 0NN, London, UK
  • Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, 98109, Seattle, Washington, USA
  • IFB Adiposity Diseases, University of Leipzig, 04103, Leipzig, Germany
  • Research Unit of Molecular Epidemiology, Helmholtz Zentrum München—German Research Center for Environmental Health, D-85764, Neuherberg, Germany
  • Department of Psychiatry, and Division of Molecular Biology and Human Genetics, Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Stellenbosch University, 7505, Tygerberg, Western Cape, South Africa
  • CHU Nantes, Service de Génétique Médicale, 44093, Nantes, France
  • Institute of Clinical Medicine, Internal Medicine, University of Eastern Finland and Kuopio University Hospital, 70210, Kuopio, Finland
  • Institute for Maternal and Child Health - IRCCS ‘Burlo Garofolo’, 34137, Trieste, Italy
  • Institute of Biomedicine & Physiology, University of Eastern Finland, 70210, Kuopio, Finland
  • Department of Genetics, University of North Carolina, Chapel Hill, 27514, North, Carolina, USA
  • Department of Biostatistical Sciences and Center for Public Health Genomics, Wake Forest School of Medicine, Winston-Salem, 27157, North, Carolina, USA
  • MRC Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, CB2 0QQ, Cambridge, UK
  • Department of Health Services, University of Washington, 98101, Seattle, Washington, USA
  • School of Medicine, Chung Shan Medical University, 402, Taichung, Taiwan
  • Division of Preventive Medicine University of Alabama at Birmingham, 35205, Birmingham, Alabama, USA
  • Key Laboratory of Nutrition and Metabolism, Institute for Nutritional Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, University of the Chinese Academy of Sciences, Shanghai, People’s Republic of China, 200031, Shanghai, China
  • Department of Medicine, Division of Cardiovascular Medicine, Stanford University School of Medicine, 94304, Palo Alto, California, USA
  • Department of Medicine, Boston University School of Medicine, 02118, Boston, Massachusetts, USA
  • Uppsala University, 75185, Uppsala, Sweden
  • Department of Experimental Medicine, Rigshospitalet, DK-2200, Copenhagen, Denmark
  • Division of Public Health Sciences, Wake Forest School of Medicine, 27157, Winston-Salem, North Carolina, USA
  • Division of Health Sciences, Warwick Medical School, Warwick University, CV4 7AL, Coventry, UK
  • Centre for Ophthalmology and Vision Science, Lions Eye Institute, University of Western Australia, 6009, Perth, Western Australia, Australia
  • Department of Psychiatry, Washington University, 63110, Saint Louis, Missouri, USA
  • Wellcome Trust Sanger Institute, Wellcome Genome Campus, CB10 1SA, Hinxton, Cambridge, UK
  • Department of Molecular Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke (DIfE), 14558, Nuthetal, Germany
  • Centre for Vision Research and Department of Ophthalmology, Westmead Millennium Institute of Medical Research, University of Sydney, 2022, Sydney, New South Wales, Australia
  • Department of Public Health and Primary Care, Leiden University Medical Center, 2300 RC, Leiden, The Netherlands
  • Centre for Global Health Research, Usher Institute of Population Health Sciences and Informatics, University of Edinburgh, EH8 9AG, Edinburgh, UK
  • DZHK (German Centre for Cardiovascular Research), partner site Munich Heart Alliance, 80802, Munich, Germany
  • Laboratory of Neurogenetics, National Institute on Aging, NIH, 20892, Bethesda, Maryland, USA
  • Institute of Clinical Chemistry and Laboratory Medicine, University Medicine Greifswald, 17475, Greifswald, Germany
  • Department of Cardiology, Heart Center, Tampere University Hospital and School of Medicine, University of Tampere, 33521, Tampere, Finland
  • Department of Medicine, Program in Personalized Medicine, University of Maryland School of Medicine, 21201, Baltimore, Maryland, USA
  • Department of Medicine, Tampere University Hospital, 33521, Tampere, Finland
  • Center for Neurobehavioral Genetics, UCLA, 90095, Los Angeles, California, USA
  • Pat Macpherson Centre for Pharmacogenetics and Pharmacogenomics, Medical Research Institute, Ninewells Hospital and Medical School, DD1 9SY, Dundee, UK
  • Division Heart & Lungs, Laboratory of Experimental Cardiology, University Medical Center Utrecht, 3584 CX, Utrecht, The Netherlands
  • School of Women’s and Infants’ Health, The University of Western Australia, 6009, Perth, Western Australia, Australia
  • University of Tartu, Estonian Genome Center, Tartu, 51010, Estonia, Tartu, Estonia
  • School of Medicine, University of Split, 21000, Split, Croatia
  • Department Clinical Genetics, Neuroscience Campus Amsterdam, VU Medical Center, 1081 HV, Amsterdam, The Netherlands
  • Research Centre of Applied and Preventive Cardiovascular Medicine, University of Turku, 20520, Turku, Finland
  • Centre for Non-Communicable Diseases, Karachi, Pakistan
  • Department of Clinical Physiology and Nuclear Medicine, Kuopio University Hospital, 70210, Kuopio, Finland
  • MRL, Merck & Co., Inc., Genetics and Pharmacogenomics, 02115, Boston, Massachusetts, USA
  • Department of Epidemiology, University of Washington, 98195, Seattle, Washington, USA
  • Department of Biobank Research, Umeå University, SE-90187, Umeå, Sweden
  • Division of Cardiovascular Medicine, Brigham and Women’s Hospital and Harvard Medical School, 02115, Boston, Massachusetts, USA
  • Department of Medicine, Faculty of Medicine, Université de Montréal, H3T 1J4, Montreal, Quebec, Canada
  • Radcliffe Department of Medicine, Oxford Centre for Diabetes, Endocrinology and Metabolism, University of Oxford, OX3 7LE, Oxford, UK
  • Department of Public Health and Clinical Medicine, Unit of Family Medicine, Umeå University, 90185, Umeå, Sweden
  • Department of Biostatistics and Epidemiology, Perelman School of Medicine, University of Pennsylvania, 19104, Philadelphia, Pennsylvania, USA
  • Division of Epidemiology & Community Health University of Minnesota, 55454, Minneapolis, Minnesota, USA
  • Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, W2 1PG, London, UK
  • Duke University, 27703, Durham, North Carolina, USA
  • Saw Swee Hock School of Public Health, National University of Singapore, National University Health System, Singapore, Singapore
  • Department of Twin Research and Genetic Epidemiology, Kingís College London, SE1 7EH, London, UK
  • Alzheimer Scotland Dementia Research Centre, University of Edinburgh, EH8 9JZ, Edinburgh, UK
  • Department of Molecular Epidemiology, Leiden University Medical Center, 2333ZC, Leiden, The Netherlands
  • MRC Integrative Epidemiology Unit, School of Social and Community Medicine, University of Bristol, BS8 2BN, Bristol, UK
  • Institute for Community Medicine, University Medicine Greifswald, 17475, Greifswald, Germany
  • Faculty of Medicine, University of Iceland, 101, Reykjavik, Iceland
  • Department for Women’s and Child Health, Center for Pediatric Research, University of Leipzig, 04103, Leipzig, Germany
  • Division of Molecular Biology and Human Genetics, Department of Biomedical Sciences, Faculty of Medicine and Health Sciences, Stellenbosch University, 7505, Tygerberg, Western Cape, South Africa
  • Department of Gerontology and Geriatrics, Leiden University Medical Center, 2333, Leiden, The Netherlands
  • Anogia Medical Centre, Anogia, Greece
  • Diabetes Research Group, King Abdulaziz University, 21589, Jeddah, Saudi Arabia
  • Department of Psychiatry, Dalhousie University, B3H 4R2, Halifax, Canada
  • Department of Brain & Cognition, University of Amsterdam, 1018 WS, Amsterdam, The Netherlands
  • Department of Epidemiology, Erasmus Medical Center, 3015 GE, Rotterdam, The Netherlands
  • Department of Epidemiology and Biostatistics, VU University Medical Center, 1007MB, Amsterdam, The Netherlands
  • Department of Cardiology, Division Heart & Lungs, University Medical Center Utrecht, Utrecht, The Netherlands
  • Department of Clinical Sciences, Genetic and Molecular Epidemiology Unit, Lund University, SE-20502, Malmö, Sweden
  • Department of Obstetrics and Gynecology, Institute for Medicine and Public Health, Vanderbilt Genetics Institute, Vanderbilt University, 37203, Nashville, Tennessee, USA
  • MRL, Merck & Co., Inc., Cardiometabolic Disease, 07033, Kenilworth, New Jersey, USA
  • Institute of Cellular Medicine, The Medical School, Newcastle University, Newcastle, NE2 4HH, UK
  • Department of Biostatistics, Boston University School of Public Health, 02118, Boston, Massachusetts, USA
  • Departments of Epidemiology & Medicine, Diabetes Translational Research Center, Fairbanks School of Public Health & School of Medicine, Indiana University, 46202, Indiana, USA
  • Department of Physiology and Biophysics, University of Mississippi Medical Center, 39216, Jackson, Mississippi, USA
  • Department of Public Health, Aarhus University, 8000, Aarhus, Denmark
  • Memorial University, Faculty of Medicine, Discipline of Genetics, St. John’s, A1B 3V6, Newfoundland, Canada
  • GlaxoSmithKlein, King of Prussia, 19406, Pennsylvania, USA
  • Department of Clinical Sciences, Quantitative Biomedical Research Center, Center for the Genetics of Host Defense, University of Texas Southwestern Medical Center, 75390, Dallas, Texas, USA
  • Department of Internal Medicine, University of Michigan, 48109, Ann Arbor, Michigan, USA
  • Department of Human Genetics, University of Michigan, 48109, Ann Arbor, Michigan, USA
  • Department of Public Health Sciences, Institute for Personalized Medicine, the Pennsylvania State University College of Medicine, 17033, Hershey, Pennsylvania, USA
  • Department of Epidemiology and Carolina Center of Genome Sciences, 27514, Chapel Hill, North Carolina, USA
  • Department of Neurology, Boston University School of Medicine, 02118, Boston, Massachusetts, USA
  • Department of Epidemiology Research, Statens Serum Institut, 2200, Copenhagen, Denmark
  • Li Ka Shing Centre for Health Information and Discovery, The Big Data Institute, University of Oxford, OX3 7BN, Oxford, UK
  • The Mindich Child Health and Development Institute, Ichan School of Medicine at Mount Sinai, 10069, New York, New York, USA
  • Departments of Pediatrics and Genetics, Harvard Medical School, 02115, Boston, Massachusetts, USA
  • Princess Al-Jawhara Al-Brahim Centre of Excellence in Research of Hereditary Disorders (PACER-HD), King Abdulaziz University, 21589, Jeddah, Saudi Arabia
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/nature21039

    DOI

    http://dx.doi.org/10.1038/nature21039

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1083401652

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/28146470


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