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A genomic approach to therapeutic target validation identifies a glucose-lowering GLP1R variant protective for coronary heart disease.

  • Scott RA Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK. dawn.m.waterworth@gsk.com robert.scott@mrc-epid.cam.ac.uk nick.wareham@mrc-epid.cam.ac.uk.
  • Freitag DF Department of Public Health and Primary Care, Strangeways Research Laboratory, University of Cambridge, Cambridge CB1 8RN, UK. The Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK.
  • Li L Statistical Genetics, Projects, Clinical Platforms, and Sciences (PCPS), GlaxoSmithKline, Research Triangle Park, NC 27709, USA.
  • Chu AY Division of Preventive Medicine, Brigham and Women's Hospital, Boston, MA 02115, USA.
  • Surendran P Department of Public Health and Primary Care, Strangeways Research Laboratory, University of Cambridge, Cambridge CB1 8RN, UK.
  • Young R Department of Public Health and Primary Care, Strangeways Research Laboratory, University of Cambridge, Cambridge CB1 8RN, UK.
  • Grarup N The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark.
  • Stancáková A Institute of Clinical Medicine, Internal Medicine, University of Eastern Finland, FI-70211 Kuopio, Finland.
  • Chen Y Department of Biostatistics, Boston University School of Public Health, Boston, MA 02118, USA.
  • Varga TV Department of Clinical Sciences, Genetic and Molecular Epidemiology Unit, Lund University, SE-205 Malmö, Sweden.
  • Yaghootkar H Genetics of Complex Traits, University of Exeter Medical School, University of Exeter, Exeter EX1 2LU, UK.
  • Luan J Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
  • Zhao JH Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
  • Willems SM Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK. Genetic Epidemiology Unit, Department of Epidemiology, Erasmus University Medical Center, 3000 CE Rotterdam, Netherlands.
  • Wessel J Department of Epidemiology, Fairbanks School of Public Health, Indianapolis, IN 46202, USA. Department of Medicine, Indiana University School of Medicine, Indianapolis, IN 46202, USA.
  • Wang S Department of Biostatistics, Boston University School of Public Health, Boston, MA 02118, USA.
  • Maruthur N Division of General Internal Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA. Welch Center for Prevention, Epidemiology, and Clinical Research, Johns Hopkins University, Baltimore, MD 21205, USA. Department of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD 21205, USA.
  • Michailidou K Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Laboratory, Worts Causeway, Cambridge CB1 8RN, UK.
  • Pirie A Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Laboratory, Worts Causeway, Cambridge CB1 8RN, UK.
  • van der Lee SJ Department of Epidemiology, Erasmus University Medical Center, 3000 CA Rotterdam, Netherlands.
  • Gillson C Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
  • Al Olama AA Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Laboratory, Worts Causeway, Cambridge CB1 8RN, UK.
  • Amouyel P University of Lille, INSERM, Centre Hospitalier Régional Universitaire de Lille, Institut Pasteur de Lille, UMR 1167, RID-AGE, F-59000 Lille, France.
  • Arriola L Public Health Division of Gipuzkoa, San Sebastian 20013, Spain. Instituto BIO-Donostia, Basque Government, San Sebastian 20014, Spain. CIBER Epidemiología y Salud Pública (CIBERESP), Madrid 28029, Spain.
  • Arveiler D Department of Epidemiology and Public Health (EA3430), University of Strasbourg, 67085 Strasbourg, France.
  • Aviles-Olmos I Sobell Department of Motor Neuroscience, UCL Institute of Neurology, London WC1N 3BG, UK.
  • Balkau B INSERM, Centre de Recherche en Epidémiologie et Santé des Populations (CESP), 94807 Villejuif, France. Univeristy of Paris-Sud, F-94805 Villejuif, France.
  • Barricarte A CIBER Epidemiología y Salud Pública (CIBERESP), Madrid 28029, Spain. Navarre Public Health Institute (ISPN), Pamplona 31003, Spain.
  • Barroso I The Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK. University of Cambridge Metabolic Research Laboratories, Wellcome Trust-MRC Institute of Metabolic Science, Cambridge CB2 0QQ, UK.
  • Garcia SB Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Laboratory, Worts Causeway, Cambridge CB1 8RN, UK.
  • Bis JC Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle, WA 98101, USA.
  • Blankenberg S Department of General and Interventional Cardiology, University Heart Center Hamburg, 20246 Hamburg, Germany.
  • Boehnke M Department of Biostatistics and Center for Statistical Genetics, University of Michigan, Ann Arbor, MI 48109-2029, USA.
  • Boeing H German Institute of Human Nutrition, Potsdam-Rehbruecke, 14558 Nuthetal, Germany.
  • Boerwinkle E Human Genetics Center, School of Public Health, University of Texas Health Science Center at Houston, Houston, TX 77025, USA. Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX 77030, USA.
  • Borecki IB Department of Genetics, Division of Statistical Genomics, Washington University School of Medicine, St. Louis, MO 63108, USA.
  • Bork-Jensen J The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark.
  • Bowden S Cancer Research UK Clinical Trials Unit, Institute for Cancer Studies, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK.
  • Caldas C Cancer Research UK Cambridge Institute and Department of Oncology, Li Ka Shing Centre, University of Cambridge, Cambridge CB2 0RE, UK.
  • Caslake M University of Glasgow, Glasgow G12 8QQ, UK.
  • Cupples LA Department of Psychiatry, Washington University School of Medicine, St. Louis, MO 63110, USA.
  • Cruchaga C Division of Statistical Genomics, Department of Genetics and Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO 63108, USA.
  • Czajkowski J Department of Medical Sciences, Molecular Epidemiology and Science for Life Laboratory, Uppsala University, SE-752 37 Uppsala, Sweden.
  • den Hoed M Warwick Clinical Trials Unit, University of Warwick, Gibbet Hill Road, Coventry CV4 7AL, UK.
  • Dunn JA University of Cambridge and National Institute of Health Research Cambridge Biomedical Research Centre, Cambridge University Hospitals National Health Service Foundation Trust, Cambridge CB2 0QQ, UK.
  • Earl HM McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD 21205, USA.
  • Ehret GB Consiglio Nazionale delle Ricerche (CNR), Institute of Clinical Physiology, 56124 Pisa, Italy.
  • Ferrannini E Department of Epidemiology, UMR 1027, INSERM, Centre Hospitalier Universitaire (CHU) de Toulouse, 31000 Toulouse, France.
  • Ferrieres J Sobell Department of Motor Neuroscience, UCL Institute of Neurology, London WC1N 3BG, UK.
  • Foltynie T University of Glasgow, Glasgow G12 8QQ, UK.
  • Ford I Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
  • Forouhi NG Department of Clinical and Experimental Medicine, Research Centre in Epidemiology and Preventive Medicine, University of Insubria, 21100 Varese, Italy. Department of Epidemiology and Prevention, Istituti di Ricovero e Cura a Carattere Scientifico (IRCCS), Istituto Neurologico Mediterraneo Neuromed, 86077 Pozzilli, Italy.
  • Gianfagna F Catalan Institute of Oncology (ICO), Barcelona 08908, Spain.
  • Gonzalez C Epidemiology and Prevention Unit, 20133 Milan, Italy.
  • Grioni S Warwick Clinical Trials Unit, University of Warwick, Gibbet Hill Road, Coventry CV4 7AL, UK.
  • Hiller L Research Unit, 931 41 Skellefteå, Sweden. Department of Public Health & Clinical Medicine, Umeå University, 901 85 Umeå, Sweden.
  • Jansson JH Steno Diabetes Center, 2820 Gentofte, Denmark. National Institute of Public Health, Southern Denmark University, DK-1353 Odense, Denmark.
  • Jørgensen ME Leiden University Medical Center, 2333 ZA Leiden, Netherlands.
  • Jukema JW German Cancer Research Centre (DKFZ), 69120 Heidelberg, Germany.
  • Kaaks R UK Clinical Research Collaboration (UKCRC) Centre of Excellence for Public Health, Queen's University Belfast, Northern Ireland, Belfast BT12 6BJ, UK.
  • Kee F Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
  • Kerrison ND University of Oxford, Oxford OX1 2JD, UK.
  • Key TJ National Institute for Health and Welfare, FI-00271 Helsinki, Finland.
  • Kontto J The Institute of Cancer Research, London SM2 5NG, UK.
  • Kote-Jarai Z Division of Statistical Genomics, Department of Genetics and Center for Genome Sciences and Systems Biology, Washington University School of Medicine, St. Louis, MO 63108, USA.
  • Kraja AT National Institute for Health and Welfare, FI-00271 Helsinki, Finland.
  • Kuulasmaa K Institute of Clinical Medicine, Internal Medicine, University of Eastern Finland, FI-70211 Kuopio, Finland. Kuopio University Hospital, FL 70029 Kuopio, Finland.
  • Kuusisto J Research Centre for Prevention and Health, Capital Region, DK-2600 Copenhagen, Denmark. Department of Clinical Experimental Research, Rigshospitalet, 2100 Glostrup, Denmark. Department of Clinical Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark.
  • Linneberg A Framingham Heart Study, Population Sciences Branch, NHLBI/National Institutes of Health (NIH), Bethesda, MD 20892, USA.
  • Liu C The Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK.
  • Marenne G Department of Genetics, University of North Carolina, Chapel Hill, NC 27599-7264, USA.
  • Mohlke KL Department of Biostatistics, University of Liverpool, Liverpool L69 3GL, UK. Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, UK.
  • Morris AP Centre for Epidemiology, Institute of Population Health, University of Manchester, Oxford Road, Manchester M13 9PT, UK. University of Warwick, Coventry CV4 7AL, UK.
  • Muir K Institute of Genetic Epidemiology, Helmholtz Zentrum München, German Research Center for Environmental Health, D-85764 Neuherberg, Germany. Department of Medicine I, Ludwig Maximilians University Munich, 80336 Munich, Germany. DZHK (German Centre for Cardiovascular Research), partner site Munich Heart Alliance, 80802 Munich, Germany.
  • Müller-Nurasyid M Clinical Pharmacology, William Harvey Research Institute, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London EC1M 6BQ, UK.
  • Munroe PB CIBER Epidemiología y Salud Pública (CIBERESP), Madrid 28029, Spain. Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia 30008, Spain.
  • Navarro C Department of Clinical Biochemistry, Herlev Hospital, Copenhagen University Hospital, University of Copenhagen, 2730 Copenhagen, Denmark.
  • Nielsen SF Lund University, 20502 Malmö, Sweden.
  • Nilsson PM Department of Clinical Biochemistry, Herlev Hospital, Copenhagen University Hospital, University of Copenhagen, 2730 Copenhagen, Denmark.
  • Nordestgaard BG University of Glasgow, Glasgow G12 8QQ, UK.
  • Packard CJ Cancer Research and Prevention Institute (ISPO), 50141 Florence, Italy.
  • Palli D Dipartimento di Medicina Clinica e Chirurgia, Federico II University, 80131 Naples, Italy.
  • Panico S Center for Human Genetic Research, Massachusetts General Hospital, Boston, MA 02114, USA. Cardiovascular Research Center, Massachusetts General Hospital, Boston, MA 02114, USA. Program in Medical and Population Genetics, Broad Institute, Cambridge, MA 02142, USA.
  • Peloso GM National Institute for Health and Welfare, FI-00271 Helsinki, Finland. Institute of Molecular Medicine Finland (FIMM), University of Helsinki, FI-00014 Helsinki, Finland.
  • Perola M DZHK (German Centre for Cardiovascular Research), partner site Munich Heart Alliance, 80802 Munich, Germany. Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, D-85764 Neuherberg, Germany.
  • Peters A University of Warwick, Coventry CV4 7AL, UK. Department of Medical Oncology, Arden Cancer Centre, University Hospital Coventry and Warwickshire, West Midlands CV2 2DX, UK.
  • Poole CJ Public Health Directorate, 33006 Oviedo, Asturias, Spain.
  • Quirós JR Umeå University, 90187 Umeå, Sweden.
  • Rolandsson O Unit of Cancer Epidemiology, Citta' della Salute e della Scienza Hospital, University of Turin, 10126 Torino, Italy. Center for Cancer Prevention (CPO), 10126 Torino, Italy. Human Genetics Foundation, 10126 Torino, Italy.
  • Sacerdote C National Institute for Health and Welfare, FI-00271 Helsinki, Finland.
  • Salomaa V CIBER Epidemiología y Salud Pública (CIBERESP), Madrid 28029, Spain. Escuela Andaluza de Salud Pública, Instituto de Investigación Biosanitaria ibs.GRANADA. Hospitales Universitarios de Granada/Universidad de Granada, Granada 18012, Spain.
  • Sánchez MJ University of Glasgow, Glasgow G12 8QQ, UK.
  • Sattar N Medical Research Council (MRC) Epidemiology Unit, University of Cambridge School of Clinical Medicine, Institute of Metabolic Science, Cambridge Biomedical Campus, Cambridge CB2 0QQ, UK.
  • Sharp SJ Institute of Psychological Medicine and Clinical Neuroscience, MRC Centre, Cardiff University, Cardiff CF24 4HQ, UK.
  • Sims R International Agency for Research on Cancer, 69372 Lyon, France.
  • Slimani N Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI 48109-2029, USA.
  • Smith JA Centre for Cancer Genetic Epidemiology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Laboratory, Worts Causeway, Cambridge CB1 8RN, UK.
  • Thompson DJ Leiden University Medical Center, 2333 ZA Leiden, Netherlands.
  • Trompet S Cancer Registry and Histopathology Unit, "Civic-M.P. Arezzo" Hospital, ASP Ragusa, 97100 Ragusa, Italy.
  • Tumino R National Institute for Public Health and the Environment (RIVM), 3720 BA Bilthoven, Netherlands.
  • van der A DL University Medical Center Utrecht, 3508 GA Utrecht, Netherlands.
  • van der Schouw YT National Institute for Health and Welfare, FI-00271 Helsinki, Finland.
  • Virtamo J Institute of Cellular Medicine, Newcastle University, Newcastle upon Tyne NE2 4HH, UK.
  • Walker M The Wellcome Trust Sanger Institute, Cambridge CB10 1SA, UK.
  • Walter K Centre for Cancer Genetic Epidemiology, Department of Oncology, University of Cambridge, Strangeways Laboratory, Worts Causeway, Cambridge CB1 8RN, UK.
  • Abraham JE Department of Clinical Sciences, Genetic and Molecular Epidemiology Unit, Lund University, SE-205 Malmö, Sweden. Department of Public Health & Clinical Medicine, Umeå University, 901 85 Umeå, Sweden. Department of Nutrition, Harvard T. H. Chan School of Public Health, Boston, MA 02115, USA.
  • Amundadottir LT Genetics of Complex Traits, University of Exeter Medical School, University of Exeter, Exeter EX1 2LU, UK.
  • Aponte JL The Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen, 2200 Copenhagen, Denmark.
  • Butterworth AS Department of Public Health and Primary Care, Strangeways Research Laboratory, University of Cambridge, Cambridge CB1 8RN, UK.
  • Dupuis J Research Centre for Prevention and Health, DK-2600 Capital Region, Denmark. Department of Public Health, Institute of Health Science, University of Copenhagen, 1014 Copenhagen, Denmark. Faculty of Medicine, Aalborg University, 9220 Aalborg, Denmark.
  • Easton DF National Heart and Lung Institute, Imperial College London, London SW3 6LY, UK. Imperial College Healthcare NHS Trust, London W2 1NY, UK. Ealing Hospital NHS Trust, Middlesex UB1 3HW, UK.
  • Eeles RA Department of Medicine, University of Kuopio, FI-70211 Kuopio, Finland.
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  • O'Rahilly S Genetics, PCPS, GlaxoSmithKline, Philadelphia, PA 19104, USA. dawn.m.waterworth@gsk.com robert.scott@mrc-epid.cam.ac.uk nick.wareham@mrc-epid.cam.ac.uk.
  • Deloukas P
  • Danesh J
  • Goodarzi MO
  • Kathiresan S
  • Meigs JB
  • Ehm MG
  • Wareham NJ
  • Waterworth DM
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  • 2016-06-03
Published in:
  • Science translational medicine. - 2016
Alleles
Coronary Disease
Diabetes Mellitus, Type 2
Dipeptidyl Peptidase 4
Genotype
Glucagon-Like Peptide-1 Receptor
Humans
Obesity
Receptor, Cannabinoid, CB2
Receptor, Serotonin, 5-HT2C
Receptors, Somatostatin
Sodium-Glucose Transporter 1
English Regulatory authorities have indicated that new drugs to treat type 2 diabetes (T2D) should not be associated with an unacceptable increase in cardiovascular risk. Human genetics may be able to guide development of antidiabetic therapies by predicting cardiovascular and other health endpoints. We therefore investigated the association of variants in six genes that encode drug targets for obesity or T2D with a range of metabolic traits in up to 11,806 individuals by targeted exome sequencing and follow-up in 39,979 individuals by targeted genotyping, with additional in silico follow-up in consortia. We used these data to first compare associations of variants in genes encoding drug targets with the effects of pharmacological manipulation of those targets in clinical trials. We then tested the association of those variants with disease outcomes, including coronary heart disease, to predict cardiovascular safety of these agents. A low-frequency missense variant (Ala316Thr; rs10305492) in the gene encoding glucagon-like peptide-1 receptor (GLP1R), the target of GLP1R agonists, was associated with lower fasting glucose and T2D risk, consistent with GLP1R agonist therapies. The minor allele was also associated with protection against heart disease, thus providing evidence that GLP1R agonists are not likely to be associated with an unacceptable increase in cardiovascular risk. Our results provide an encouraging signal that these agents may be associated with benefit, a question currently being addressed in randomized controlled trials. Genetic variants associated with metabolic traits and multiple disease outcomes can be used to validate therapeutic targets at an early stage in the drug development process.
Language
  • English
Open access status
green
Identifiers
Persistent URL
https://sonar.ch/global/documents/126234
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