Low-frequency and rare exome chip variants associate with fasting glucose and type 2 diabetes susceptibility

Jennifer Wessel; Audrey Y Chu; Sara M Willems; Shuai Wang; Hanieh Yaghootkar; Jennifer A Brody; Marco Dauriz; Marie-France Hivert; Sridharan Raghavan; Leonard Lipovich; Bertha Hidalgo; Keolu Fox; Jennifer E Huffman; Ping An; Yingchang Lu; Laura J Rasmussen-Torvik; Niels Grarup; Margaret G Ehm; Li Li; Abigail S Baldridge; Alena Stančáková; Ravinder Abrol; Céline Besse; Anne Boland; Jette Bork-Jensen; Myriam Fornage; Daniel F Freitag; Melissa E Garcia; Xiuqing Guo; Kazuo Hara; Aaron Isaacs; Johanna Jakobsdottir; Leslie A Lange; Jill C Layton; Man Li; Jing Hua Zhao; Karina Meidtner; Alanna C Morrison; Mike A Nalls; Marjolein J Peters; Maria Sabater-Lleal; Claudia Schurmann; Angela Silveira; Albert V Smith; Lorraine Southam; Marcus H Stoiber; Rona J Strawbridge; Kent D Taylor; Tibor V Varga; Kristine H Allin; Najaf Amin; Jennifer L Aponte; Tin Aung; Caterina Barbieri; Nathan A Bihlmeyer; Michael Boehnke; Cristina Bombieri; Donald W Bowden; Sean M Burns; Yuning Chen; Yii-DerI Chen; Ching-Yu Cheng; Adolfo Correa; Jacek Czajkowski; Abbas Dehghan; Georg B Ehret; Gudny Eiriksdottir; Stefan A Escher; Aliki-Eleni Farmaki; Mattias Frånberg; Giovanni Gambaro; Franco Giulianini; William A Goddard, 3rd; Anuj Goel; Omri Gottesman; Megan L Grove; Stefan Gustafsson; Yang Hai; Göran Hallmans; Jiyoung Heo; Per Hoffmann; Mohammad K Ikram; Richard A Jensen; Marit E Jørgensen; Torben Jørgensen; Maria Karaleftheri; Chiea C Khor; Andrea Kirkpatrick; Aldi T Kraja; Johanna Kuusisto; Ethan M Lange; I T Lee; Wen-Jane Lee; Aaron Leong; Jiemin Liao; Chunyu Liu; Yongmei Liu; Cecilia M Lindgren; Allan Linneberg; Giovanni Malerba; Vasiliki Mamakou; Eirini Marouli; Nisa M Maruthur; Angela Matchan; Roberta McKean-Cowdin; Olga McLeod; Ginger A Metcalf; Karen L Mohlke; Donna M Muzny; Ioanna Ntalla; Nicholette D Palmer; Dorota Pasko; Andreas Peter; Nigel W Rayner; Frida Renström; Ken Rice; Cinzia F Sala; Bengt Sennblad; Ioannis Serafetinidis; Jennifer A Smith; Nicole Soranzo; Elizabeth K Speliotes; Eli A Stahl; Kathleen Stirrups; Nikos Tentolouris; Anastasia Thanopoulou; Mina Torres; Michela Traglia; Emmanouil Tsafantakis; Sundas Javad; Lisa R Yanek; Eleni Zengini; Diane M Becker; Joshua C Bis; James B Brown; L Adrienne Cupples; Torben Hansen; Erik Ingelsson; Andrew J Karter; Carlos Lorenzo; Rasika A Mathias; Jill M Norris; Gina M Peloso; Wayne H-H Sheu; Daniela Toniolo; Dhananjay Vaidya; Rohit Varma; Lynne E Wagenknecht; Heiner Boeing; Erwin P Bottinger; George Dedoussis; Panos Deloukas; Ele Ferrannini; Oscar H Franco; Paul W Franks; Richard A Gibbs; Vilmundur Gudnason; Anders Hamsten; Tamara B Harris; Andrew T Hattersley; Caroline Hayward; Albert Hofman; Jan-Håkan Jansson; Claudia Langenberg; Lenore J Launer; Daniel Levy; Ben A Oostra; Christopher J O'Donnell; Stephen O'Rahilly; Sandosh Padmanabhan; James S Pankow; Ozren Polasek; Michael A Province; Stephen S Rich; Paul M Ridker; Igor Rudan; Matthias B Schulze; Blair H Smith; André G Uitterlinden; Mark Walker; Hugh Watkins; Tien Y Wong; Eleftheria Zeggini; Markku Laakso; Ingrid B Borecki; Daniel I Chasman; Oluf Pedersen; Bruce M Psaty; E Shyong Tai; Cornelia M van Duijn; Nicholas J Wareham; Dawn M Waterworth; Eric Boerwinkle; W H Linda Kao; Jose C Florez; Ruth J F Loos; James G Wilson; Timothy M Frayling; David S Siscovick; Josée Dupuis; Jerome I Rotter; James B Meigs; Robert A Scott; Mark O Goodarzi; EPIC-InterAct Consortium

doi:10.1038/ncomms6897

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Low-frequency and rare exome chip variants associate with fasting glucose and type 2 diabetes susceptibility

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Low-frequency and rare exome chip variants associate with fasting glucose and type 2 diabetes susceptibility

Jennifer Wessel, Audrey Y Chu, Sara M Willems, Shuai Wang, Hanieh Yaghootkar, Jennifer A Brody, Marco Dauriz, Marie-France Hivert, Sridharan Raghavan, Leonard Lipovich, …

Nature communications, Vol.6(1), pp.5897-5897

01/01/2015

DOI: https://doi.org/10.1038/ncomms6897

PMCID: PMC4311266

PMID: 25631608

Abstract

Blacks - genetics

Blood Glucose - metabolism

Diabetes Mellitus, Type 2 - blood

Diabetes Mellitus, Type 2 - genetics

Exome - genetics

Fasting - blood

Genetic Association Studies

Genetic Loci

Genetic Predisposition to Disease

Genetic Variation

Glucagon-Like Peptide-1 Receptor - genetics

Glucose-6-Phosphatase - genetics

Humans

Insulin - blood

Mutation Rate

Oligonucleotide Array Sequence Analysis

Polymorphism, Single Nucleotide - genetics

Whites - genetics

Fasting glucose and insulin are intermediate traits for type 2 diabetes. Here we explore the role of coding variation on these traits by analysis of variants on the HumanExome BeadChip in 60,564 non-diabetic individuals and in 16,491 T2D cases and 81,877 controls. We identify a novel association of a low-frequency nonsynonymous SNV in GLP1R (A316T; rs10305492; MAF=1.4%) with lower FG (β=-0.09±0.01 mmol l(-1), P=3.4 × 10(-12)), T2D risk (OR[95%CI]=0.86[0.76-0.96], P=0.010), early insulin secretion (β=-0.07±0.035 pmolinsulin mmolglucose(-1), P=0.048), but higher 2-h glucose (β=0.16±0.05 mmol l(-1), P=4.3 × 10(-4)). We identify a gene-based association with FG at G6PC2 (pSKAT=6.8 × 10(-6)) driven by four rare protein-coding SNVs (H177Y, Y207S, R283X and S324P). We identify rs651007 (MAF=20%) in the first intron of ABO at the putative promoter of an antisense lncRNA, associating with higher FG (β=0.02±0.004 mmol l(-1), P=1.3 × 10(-8)). Our approach identifies novel coding variant associations and extends the allelic spectrum of variation underlying diabetes-related quantitative traits and T2D susceptibility.

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Title: Low-frequency and rare exome chip variants associate with fasting glucose and type 2 diabetes susceptibility
Creators - without role: Jennifer Wessel - Indiana University
Audrey Y Chu - National Heart Lung and Blood Institute
Sara M Willems - Erasmus MC
Shuai Wang - Boston University
Hanieh Yaghootkar - University of Exeter
Jennifer A Brody - University of Washington
Marco Dauriz - University of Verona
Marie-France Hivert - Harvard Pilgrim Health Care
Sridharan Raghavan - Harvard Medical School
Leonard Lipovich - Wayne State University
Bertha Hidalgo - University of Alabama at Birmingham
Keolu Fox - University of Washington
Jennifer E Huffman - University of Edinburgh
Ping An - Division of Statistical Genomics and Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63108, USA
Yingchang Lu - Icahn School of Medicine at Mount Sinai
Laura J Rasmussen-Torvik - Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611, USA
Niels Grarup - University of Copenhagen
Margaret G Ehm - GlaxoSmithKline
Li Li - Quantitative Sciences, PCPS, GlaxoSmithKline, North Carolina 27709, USA
Abigail S Baldridge - Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, Illinois 60611, USA
Alena Stančáková - University of Eastern Finland
Ravinder Abrol - Cedars-Sinai Medical Center
Céline Besse - Evry
Anne Boland - Evry
Jette Bork-Jensen - University of Copenhagen
Myriam Fornage - Brown Foundation Institute of Molecular Medicine, University of Texas Health Science Center, Houston, Texas 77030, USA
Daniel F Freitag - University of Cambridge
Melissa E Garcia - National Institute on Aging
Xiuqing Guo - The Lundquist Institute
Kazuo Hara - Icahn School of Medicine at Mount Sinai
Aaron Isaacs - Erasmus MC
Johanna Jakobsdottir - Icelandic Heart Association
Leslie A Lange - Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599, USA
Jill C Layton - Indiana University
Man Li - Johns Hopkins University
Jing Hua Zhao - University of Cambridge
Karina Meidtner - German Institute of Human Nutrition
Alanna C Morrison - The University of Texas Health Science Center at Houston
Mike A Nalls - National Institute on Aging
Marjolein J Peters - Erasmus MC
Maria Sabater-Lleal - Karolinska Institutet
Claudia Schurmann - Icahn School of Medicine at Mount Sinai
Angela Silveira - Karolinska Institutet
Albert V Smith - University of Iceland
Lorraine Southam - Wellcome Centre for Human Genetics
Marcus H Stoiber - Lawrence Berkeley National Laboratory
Rona J Strawbridge - Karolinska Institutet
Kent D Taylor - The Lundquist Institute
Tibor V Varga - Skåne University Hospital
Kristine H Allin - University of Copenhagen
Najaf Amin - Erasmus MC
Jennifer L Aponte - GlaxoSmithKline
Tin Aung - Duke-NUS Medical School
Caterina Barbieri - Division of Genetics and Cell Biology, San Raffaele Research Institute, Milano 20132, Italy
Nathan A Bihlmeyer - Johns Hopkins University School of Medicine
Michael Boehnke - University of Michigan–Ann Arbor
Cristina Bombieri - University of Verona
Donald W Bowden - Department of Biochemistry, Wake Forest School of Medicine, Winston-Salem, North Carolina 27157, USA
Sean M Burns - Massachusetts General Hospital
Yuning Chen - Boston University
Yii-DerI Chen - The Lundquist Institute
Ching-Yu Cheng - Duke-NUS Medical School
Adolfo Correa - University of Mississippi Medical Center
Jacek Czajkowski - Division of Statistical Genomics and Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63108, USA
Abbas Dehghan - Erasmus MC
Georg B Ehret - Johns Hopkins University
Gudny Eiriksdottir - Icelandic Heart Association
Stefan A Escher - Skåne University Hospital
Aliki-Eleni Farmaki - Harokopio University of Athens
Mattias Frånberg - Stockholm University
Giovanni Gambaro - Pontifícia Universidade Católica de São Paulo
Franco Giulianini - Brigham and Women's Hospital
William A Goddard, 3rd - Materials and Process Simulation Center, California Institute of Technology, Pasadena, California 91125, USA
Anuj Goel - University of Oxford
Omri Gottesman - Icahn School of Medicine at Mount Sinai
Megan L Grove - The University of Texas Health Science Center at Houston
Stefan Gustafsson - Uppsala University
Yang Hai - The Lundquist Institute
Göran Hallmans - Umeå University
Jiyoung Heo - Sangmyung University
Per Hoffmann - University Hospital of Basel
Mohammad K Ikram - 1] Singapore Eye Research Institute, Singapore National Eye Centre, Singapore 168751, Singapore Office of Clinical Sciences, Duke-NUS Graduate Medical School, National University of Singapore, Singapore 169857, Singapore Memory Aging &Cognition Centre (MACC), National University Health System, Singapore 117599, Singapore
Richard A Jensen - University of Washington
Marit E Jørgensen - Steno Diabetes Center
Torben Jørgensen - 1] Research Centre for Prevention and Health, Glostrup University Hospital, Glostrup DK-2600, Denmark Faculty of Medicine, University of Aalborg, Aalborg DK-9220, Denmark
Maria Karaleftheri - Echinos Medical Centre, Echinos 67300, Greece
Chiea C Khor - Duke-NUS Medical School
Andrea Kirkpatrick - Materials and Process Simulation Center, California Institute of Technology, Pasadena, California 91125, USA
Aldi T Kraja - Division of Statistical Genomics and Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63108, USA
Johanna Kuusisto - University of Eastern Finland
Ethan M Lange - 1] Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599, USA Department of Biostatistics, University of North Carolina, Chapel Hill, North Carolina 27599, USA
I T Lee - National Yang Ming University
Wen-Jane Lee - Taichung Veterans General Hospital
Aaron Leong - Harvard Medical School
Jiemin Liao - 1] Singapore Eye Research Institute, Singapore National Eye Centre, Singapore 168751, Singapore Department of Ophthalmology, National University of Singapore and National University Health System, Singapore 119228, Singapore
Chunyu Liu - National Heart Lung and Blood Institute
Yongmei Liu - Wake Forest University
Cecilia M Lindgren - University of Oxford
Allan Linneberg - Copenhagen University Hospital
Giovanni Malerba - University of Verona
Vasiliki Mamakou - National and Kapodistrian University of Athens
Eirini Marouli - Harokopio University of Athens
Nisa M Maruthur - Johns Hopkins University School of Medicine
Angela Matchan - Wellcome Sanger Institute
Roberta McKean-Cowdin - Department of Preventive Medicine, Keck School of Medicine of the University of Southern California, Los Angeles 90033, USA
Olga McLeod - Karolinska Institutet
Ginger A Metcalf - Baylor College of Medicine
Karen L Mohlke - Department of Genetics, University of North Carolina, Chapel Hill, North Carolina 27599, USA
Donna M Muzny - Baylor College of Medicine
Ioanna Ntalla - Harokopio University of Athens
Nicholette D Palmer - Genomics
Dorota Pasko - University of Exeter
Andreas Peter - University of Tübingen
Nigel W Rayner - University of Oxford
Frida Renström - Skåne University Hospital
Ken Rice - University of Washington
Cinzia F Sala - Division of Genetics and Cell Biology, San Raffaele Research Institute, Milano 20132, Italy
Bengt Sennblad - Karolinska Institutet
Ioannis Serafetinidis - Department of Gastroenterology, Gennimatas General Hospital, Athens 11527, Greece
Jennifer A Smith - University of Michigan–Ann Arbor
Nicole Soranzo - Wellcome Sanger Institute
Elizabeth K Speliotes - University of Michigan–Ann Arbor
Eli A Stahl - Icahn School of Medicine at Mount Sinai
Kathleen Stirrups - Queen Mary University of London
Nikos Tentolouris - Laiko General Hospital of Athens
Anastasia Thanopoulou - National and Kapodistrian University of Athens
Mina Torres - Department of Preventive Medicine, Keck School of Medicine of the University of Southern California, Los Angeles 90033, USA
Michela Traglia - Division of Genetics and Cell Biology, San Raffaele Research Institute, Milano 20132, Italy
Emmanouil Tsafantakis - Anogia Medical Centre, Anogia 740 51, Greece
Sundas Javad - University of Cambridge
Lisa R Yanek - Johns Hopkins University School of Medicine
Eleni Zengini - University of Sheffield
Diane M Becker - Johns Hopkins University School of Medicine
Joshua C Bis - University of Washington
James B Brown - University of California, Berkeley
L Adrienne Cupples - Boston University
Torben Hansen - University of Copenhagen
Erik Ingelsson - Uppsala University
Andrew J Karter - Kaiser Permanente
Carlos Lorenzo - Department of Medicine, University of Texas Health Science Center, San Antonio, Texas 77030, USA
Rasika A Mathias - Johns Hopkins University School of Medicine
Jill M Norris - University of Colorado Denver
Gina M Peloso - Massachusetts General Hospital
Wayne H-H Sheu - National Yang Ming University
Daniela Toniolo - Division of Genetics and Cell Biology, San Raffaele Research Institute, Milano 20132, Italy
Dhananjay Vaidya - Johns Hopkins University School of Medicine
Rohit Varma - Department of Preventive Medicine, Keck School of Medicine of the University of Southern California, Los Angeles 90033, USA
Lynne E Wagenknecht - Division of Public Health Sciences, Wake Forest School of Medicine, Winston-Salem, North Carolina 27106, USA
Heiner Boeing - German Institute of Human Nutrition
Erwin P Bottinger - Icahn School of Medicine at Mount Sinai
George Dedoussis - Harokopio University of Athens
Panos Deloukas - Queen Mary University of London
Ele Ferrannini - Istituto di Fisiologia Clinica
Oscar H Franco - Erasmus MC
Paul W Franks - Skåne University Hospital
Richard A Gibbs - Baylor College of Medicine
Vilmundur Gudnason - University of Iceland
Anders Hamsten - Karolinska Institutet
Tamara B Harris - National Institute on Aging
Andrew T Hattersley - University of Exeter
Caroline Hayward - University of Edinburgh
Albert Hofman - Erasmus MC
Jan-Håkan Jansson - Umeå University
Claudia Langenberg - University of Cambridge
Lenore J Launer - National Institute on Aging
Daniel Levy - National Heart Lung and Blood Institute
Ben A Oostra - Erasmus MC
Christopher J O'Donnell - National Heart Lung and Blood Institute
Stephen O'Rahilly - University of Cambridge
Sandosh Padmanabhan - University of Glasgow
James S Pankow - University of Minnesota
Ozren Polasek - University of Split
Michael A Province - Division of Statistical Genomics and Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63108, USA
Stephen S Rich - University of Virginia
Paul M Ridker - Brigham and Women's Hospital
Igor Rudan - University of Edinburgh
Matthias B Schulze - German Center for Diabetes Research
Blair H Smith - University of Dundee
André G Uitterlinden - Erasmus MC
Mark Walker - Newcastle University
Hugh Watkins - University of Oxford
Tien Y Wong - Duke-NUS Medical School
Eleftheria Zeggini - Wellcome Sanger Institute
Markku Laakso - University of Eastern Finland
Ingrid B Borecki - Division of Statistical Genomics and Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63108, USA
Daniel I Chasman - Brigham and Women's Hospital
Oluf Pedersen - University of Copenhagen
Bruce M Psaty - University of Washington
E Shyong Tai - National University of Singapore
Cornelia M van Duijn - Erasmus MC
Nicholas J Wareham - University of Cambridge
Dawn M Waterworth - GlaxoSmithKline
Eric Boerwinkle - The University of Texas Health Science Center at Houston
W H Linda Kao - Johns Hopkins University
Jose C Florez - Harvard Medical School
Ruth J F Loos - Icahn School of Medicine at Mount Sinai
James G Wilson - University of Mississippi Medical Center
Timothy M Frayling - University of Exeter
David S Siscovick - University of Washington
Josée Dupuis - Boston University
Jerome I Rotter - The Lundquist Institute
James B Meigs - Harvard Medical School
Robert A Scott - University of Cambridge
Mark O Goodarzi - Cedars-Sinai Medical Center
EPIC-InterAct Consortium
Publication Details: Nature communications, Vol.6(1), pp.5897-5897
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Identifiers: 9937138408331
Academic Unit: King Abdulaziz University
Language: English
Resource Type: Journal article