Exome Chip Meta-analysis Fine Maps Causal Variants and Elucidates the Genetic Architecture of Rare Coding Variants in Smoking and Alcohol Use.


Journal

Biological psychiatry
ISSN: 1873-2402
Titre abrégé: Biol Psychiatry
Pays: United States
ID NLM: 0213264

Informations de publication

Date de publication:
01 06 2019
Historique:
received: 15 09 2017
revised: 05 11 2018
accepted: 29 11 2018
pubmed: 27 1 2019
medline: 14 4 2020
entrez: 26 1 2019
Statut: ppublish

Résumé

Smoking and alcohol use have been associated with common genetic variants in multiple loci. Rare variants within these loci hold promise in the identification of biological mechanisms in substance use. Exome arrays and genotype imputation can now efficiently genotype rare nonsynonymous and loss of function variants. Such variants are expected to have deleterious functional consequences and to contribute to disease risk. We analyzed ∼250,000 rare variants from 16 independent studies genotyped with exome arrays and augmented this dataset with imputed data from the UK Biobank. Associations were tested for five phenotypes: cigarettes per day, pack-years, smoking initiation, age of smoking initiation, and alcoholic drinks per week. We conducted stratified heritability analyses, single-variant tests, and gene-based burden tests of nonsynonymous/loss-of-function coding variants. We performed a novel fine-mapping analysis to winnow the number of putative causal variants within associated loci. Meta-analytic sample sizes ranged from 152,348 to 433,216, depending on the phenotype. Rare coding variation explained 1.1% to 2.2% of phenotypic variance, reflecting 11% to 18% of the total single nucleotide polymorphism heritability of these phenotypes. We identified 171 genome-wide associated loci across all phenotypes. Fine mapping identified putative causal variants with double base-pair resolution at 24 of these loci, and between three and 10 variants for 65 loci. Twenty loci contained rare coding variants in the 95% credible intervals. Rare coding variation significantly contributes to the heritability of smoking and alcohol use. Fine-mapping genome-wide association study loci identifies specific variants contributing to the biological etiology of substance use behavior.

Sections du résumé

BACKGROUND
Smoking and alcohol use have been associated with common genetic variants in multiple loci. Rare variants within these loci hold promise in the identification of biological mechanisms in substance use. Exome arrays and genotype imputation can now efficiently genotype rare nonsynonymous and loss of function variants. Such variants are expected to have deleterious functional consequences and to contribute to disease risk.
METHODS
We analyzed ∼250,000 rare variants from 16 independent studies genotyped with exome arrays and augmented this dataset with imputed data from the UK Biobank. Associations were tested for five phenotypes: cigarettes per day, pack-years, smoking initiation, age of smoking initiation, and alcoholic drinks per week. We conducted stratified heritability analyses, single-variant tests, and gene-based burden tests of nonsynonymous/loss-of-function coding variants. We performed a novel fine-mapping analysis to winnow the number of putative causal variants within associated loci.
RESULTS
Meta-analytic sample sizes ranged from 152,348 to 433,216, depending on the phenotype. Rare coding variation explained 1.1% to 2.2% of phenotypic variance, reflecting 11% to 18% of the total single nucleotide polymorphism heritability of these phenotypes. We identified 171 genome-wide associated loci across all phenotypes. Fine mapping identified putative causal variants with double base-pair resolution at 24 of these loci, and between three and 10 variants for 65 loci. Twenty loci contained rare coding variants in the 95% credible intervals.
CONCLUSIONS
Rare coding variation significantly contributes to the heritability of smoking and alcohol use. Fine-mapping genome-wide association study loci identifies specific variants contributing to the biological etiology of substance use behavior.

Identifiants

pubmed: 30679032
pii: S0006-3223(18)32056-0
doi: 10.1016/j.biopsych.2018.11.024
pmc: PMC6534468
mid: NIHMS1519259
pii:
doi:

Types de publication

Journal Article Meta-Analysis Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

946-955

Subventions

Organisme : NIDA NIH HHS
ID : T32 DA017637
Pays : United States
Organisme : Medical Research Council
ID : MR/L003120/1
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : U01 AG009740
Pays : United States
Organisme : British Heart Foundation
ID : RG/13/13/30194
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM126479
Pays : United States
Organisme : Medical Research Council
ID : MR/N01104X/2
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N01104X/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1000861
Pays : United Kingdom
Organisme : NIDA NIH HHS
ID : R01 DA037904
Pays : United States
Organisme : Medical Research Council
ID : MR/S003762/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_17228
Pays : United Kingdom
Organisme : NIAAA NIH HHS
ID : R37 AA009367
Pays : United States
Organisme : Medical Research Council
ID : MC_UU_12015/1
Pays : United Kingdom
Organisme : NIDA NIH HHS
ID : R21 DA040177
Pays : United States
Organisme : Medical Research Council
ID : G1001799
Pays : United Kingdom
Organisme : Medical Research Council
ID : G0700704
Pays : United Kingdom
Organisme : NHLBI NIH HHS
ID : R01 HL119443
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK062370
Pays : United States
Organisme : Medical Research Council
ID : MC_PC_12010
Pays : United Kingdom
Organisme : NHGRI NIH HHS
ID : R01 HG008983
Pays : United States
Organisme : NIDA NIH HHS
ID : R01 DA042755
Pays : United States
Organisme : Medical Research Council
ID : MR/S003746/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00007/10
Pays : United Kingdom
Organisme : NIDDK NIH HHS
ID : U01 DK062370
Pays : United States
Organisme : NIH HHS
ID : S10 OD020069
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_QA137853
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K026992/1
Pays : United Kingdom

Investigateurs

Praveen Surendran (P)
Robin Young (R)
Daniel R Barnes (DR)
Sune Fallgaard Nielsen (SF)
Asif Rasheed (A)
Maria Samuel (M)
Wei Zhao (W)
Jukka Kontto (J)
Markus Perola (M)
Muriel Caslake (M)
Anton J M de Craen (AJM)
Stella Trompet (S)
Maria Uria-Nickelsen (M)
Anders Malarstig (A)
Dermot F Reily (DF)
Maarten Hoek (M)
Thomas Vogt (T)
J Wouter Jukema (JW)
Naveed Sattar (N)
Ian Ford (I)
Chris J Packard (CJ)
Dewan S Alam (DS)
Abdulla Al Shafi Majumder (AAS)
Emanuele Di Angelantonio (E)
Rajiv Chowdhury (R)
Philippe Amouyel (P)
Dominique Arveiler (D)
Stefan Blankenberg (S)
Jean Ferrières (J)
Frank Kee (F)
Kari Kuulasmaa (K)
Martina Müller-Nurasyid (M)
Giovanni Veronesi (G)
Jarmo Virtamo (J)
None Epic-Cvd Consortium
Philippe Frossard (P)
Børge Grønne Nordestgaard (BG)
Danish Saleheen (D)
John Danesh (J)
Adam S Butterworth (AS)
Joanna M M Howson (JMM)
A Mesut Erzurumluoglu (AM)
Victoria E Jackson (VE)
Carl A Melbourne (CA)
Tibor V Varga (TV)
Helen R Warren (HR)
Vinicius Tragante (V)
Ioanna Tachmazidou (I)
Sarah E Harris (SE)
Evangelos Evangelou (E)
Jonathan Marten (J)
Weihua Zhang (W)
Elisabeth Altmaier (E)
Jian'an Luan (J)
Claudia Langenberg (C)
Robert A Scott (RA)
Hanieh Yaghootkar (H)
Kathleen Stirrups (K)
Stavroula Kanoni (S)
Eirini Marouli (E)
Fredrik Karpe (F)
Anna F Dominiczak (AF)
Peter Sever (P)
Neil Poulter (N)
Olov Rolandsson (O)
Clemens Baumbach (C)
Saima Afaq (S)
John C Chambers (JC)
Jaspal S Kooner (JS)
Nicholas J Wareham (NJ)
Frida Renström (F)
Göran Hallmans (G)
Riccardo E Marioni (RE)
Janie Corley (J)
John M Starr (JM)
Niek Verweij (N)
Rudolf A de Boer (RA)
Peter van der Meer (P)
Ersin Yavas (E)
Ilonca Vaartjes (I)
Michiel L Bots (ML)
Folkert W Asselbergs (FW)
Hans J Grabe (HJ)
Henry Völzke (H)
Matthias Nauck (M)
Stefan Weiss (S)
Paul D P Pharoah (PDP)
Alison M Dunning (AM)
Joe G Dennis (JG)
Deborah J Thompson (DJ)
Kyriaki Michailidou (K)
Douglas F Easton (DF)
Antonis C Antoniou (AC)
Jessica Tyrrell (J)
Evelin Mihailov (E)
Nilesh J Samani (NJ)
Kaixin Zhou (K)
Matthew J Neville (MJ)
Andres Metspalu (A)
Colin N A Palmer (CNA)
Ian P Hall (IP)
David P Strachan (DP)
Ian J Deary (IJ)
Tim M Frayling (TM)
Caroline Hayward (C)
Pim van der Harst (P)
Eleftheria Zeggini (E)
None Understanding Society Scientific Group
Patricia B Munroe (PB)
Jan-Håkan Jansson (JH)
Paul W Franks (PW)
Panos Deloukas (P)
Mark J Caulfield (MJ)
Louise V Wain (LV)
Martin D Tobin (MD)

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2018 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

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Auteurs

David M Brazel (DM)

Institute for Behavioral Genetics, University of Colorado Boulder, Boulder, Colorado; Department of Molecular, Cellular, and Developmental Biology, University of Colorado Boulder, Boulder, Colorado.

Yu Jiang (Y)

Department of Public Health Sciences, Penn State College of Medicine, Hershey, Pennsylvania.

Jordan M Hughey (JM)

Department of Public Health Sciences, Penn State College of Medicine, Hershey, Pennsylvania.

Valérie Turcot (V)

Department of Medicine, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada; Montreal Heart Institute, Montreal, Quebec, Canada.

Xiaowei Zhan (X)

Department of Clinical Science, Center for Genetics of Host Defense, University of Texas Southwestern, Dallas, Texas.

Jian Gong (J)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Chiara Batini (C)

Department of Health Sciences, University of Leicester, Leicester, United Kingdom.

J Dylan Weissenkampen (JD)

Department of Public Health Sciences, Penn State College of Medicine, Hershey, Pennsylvania.

MengZhen Liu (M)

Department of Psychology, University of Minnesota, Minneapolis, Minnesota.

Daniel R Barnes (DR)

Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.

Sarah Bertelsen (S)

Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, New York.

Yi-Ling Chou (YL)

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri.

A Mesut Erzurumluoglu (AM)

Department of Health Sciences, University of Leicester, Leicester, United Kingdom.

Jessica D Faul (JD)

Survey Research Center, Institute for Social Research, University of Michigan, Ann Arbor, Michigan.

Jeff Haessler (J)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Anke R Hammerschlag (AR)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam, University of Amsterdam, Amsterdam, the Netherlands.

Chris Hsu (C)

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

Manav Kapoor (M)

Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, New York.

Dongbing Lai (D)

Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, Indiana.

Nhung Le (N)

Department of Medical Microbiology, Immunology and Cell Biology, Southern Illinois University School of Medicine, Springfield, Illinois.

Christiaan A de Leeuw (CA)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam, University of Amsterdam, Amsterdam, the Netherlands.

Anu Loukola (A)

Institute for Molecular Medicine Finland, University of Helsinki, Helsinki, Finland; Department of Public Health, University of Helsinki, Helsinki, Finland.

Massimo Mangino (M)

Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom; National Institute for Health Research Biomedical Research Centre at Guy's and St Thomas' Foundation Trust, London, United Kingdom.

Carl A Melbourne (CA)

Department of Health Sciences, University of Leicester, Leicester, United Kingdom.

Giorgio Pistis (G)

Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato, Italy.

Beenish Qaiser (B)

Institute for Molecular Medicine Finland, University of Helsinki, Helsinki, Finland; Department of Public Health, University of Helsinki, Helsinki, Finland.

Rebecca Rohde (R)

Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.

Yaming Shao (Y)

Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.

Heather Stringham (H)

Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, Michigan.

Leah Wetherill (L)

Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, Indiana.

Wei Zhao (W)

Department of Epidemiology, University of Michigan, Ann Arbor, Michigan.

Arpana Agrawal (A)

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri.

Laura Bierut (L)

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri.

Chu Chen (C)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington; Department of Epidemiology, Head and Neck Surgery Center, University of Washington, Seattle, Washington; Department of Otolaryngology, Head and Neck Surgery Center, University of Washington, Seattle, Washington.

Charles B Eaton (CB)

Department of Family Medicine, Brown University, Providence, Rhode Island.

Alison Goate (A)

Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, New York.

Christopher Haiman (C)

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

Andrew Heath (A)

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri.

William G Iacono (WG)

Department of Psychology, University of Minnesota, Minneapolis, Minnesota.

Nicholas G Martin (NG)

Queensland Institute for Medical Research, Brisbane, Australia.

Tinca J Polderman (TJ)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam, University of Amsterdam, Amsterdam, the Netherlands.

Alex Reiner (A)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington; Department of Epidemiology, Head and Neck Surgery Center, University of Washington, Seattle, Washington.

John Rice (J)

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri; Department of Mathematics, Washington University in St. Louis, St. Louis, Missouri.

David Schlessinger (D)

National Institute on Aging, National Institutes of Health, Bethesda, Maryland.

H Steven Scholte (HS)

Department of Psychology, University of Amsterdam, Amsterdam, the Netherlands; Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, the Netherlands.

Jennifer A Smith (JA)

Department of Epidemiology, University of Michigan, Ann Arbor, Michigan.

Jean-Claude Tardif (JC)

Department of Medicine, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada; Montreal Heart Institute, Montreal, Quebec, Canada.

Hilary A Tindle (HA)

Department of Medicine, Vanderbilt University, Nashville, Tennessee.

Andries R van der Leij (AR)

Department of Psychology, University of Amsterdam, Amsterdam, the Netherlands; Amsterdam Brain and Cognition, University of Amsterdam, Amsterdam, the Netherlands.

Michael Boehnke (M)

Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, Michigan.

Jenny Chang-Claude (J)

Division of Cancer Epidemiology, German Cancer Research Center, Heidelberg, Germany.

Francesco Cucca (F)

Istituto di Ricerca Genetica e Biomedica, Consiglio Nazionale delle Ricerche, Monserrato, Italy.

Sean P David (SP)

Department of Medicine, Stanford University, Stanford, California.

Tatiana Foroud (T)

Department of Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, Indiana.

Joanna M M Howson (JMM)

Department of Public Health and Primary Care, University of Cambridge, Cambridge, United Kingdom.

Sharon L R Kardia (SLR)

Department of Epidemiology, University of Michigan, Ann Arbor, Michigan.

Charles Kooperberg (C)

Public Health Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, Washington.

Markku Laakso (M)

Department of Internal Medicine, Institute of Clinical Medicine, University of Eastern Finland, Kuopio, Finland.

Guillaume Lettre (G)

Department of Medicine, Faculty of Medicine, Université de Montréal, Montreal, Quebec, Canada; Montreal Heart Institute, Montreal, Quebec, Canada.

Pamela Madden (P)

Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri.

Matt McGue (M)

Department of Psychology, University of Minnesota, Minneapolis, Minnesota.

Kari North (K)

Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.

Danielle Posthuma (D)

Department of Complex Trait Genetics, Center for Neurogenomics and Cognitive Research, Amsterdam Neuroscience, VU University Amsterdam, University of Amsterdam, Amsterdam, the Netherlands; Department of Clinical Genetics, VU University Medical Centre, University of Amsterdam, Amsterdam, the Netherlands.

Timothy Spector (T)

Department of Twin Research and Genetic Epidemiology, King's College London, London, United Kingdom.

Daniel Stram (D)

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

Martin D Tobin (MD)

Department of Health Sciences, University of Leicester, Leicester, United Kingdom.

David R Weir (DR)

Survey Research Center, Institute for Social Research, University of Michigan, Ann Arbor, Michigan.

Jaakko Kaprio (J)

Institute for Molecular Medicine Finland, University of Helsinki, Helsinki, Finland; Department of Public Health, University of Helsinki, Helsinki, Finland.

Gonçalo R Abecasis (GR)

Regeneron Pharmaceuticals, Tarrytown, New York; Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, Michigan.

Dajiang J Liu (DJ)

Institute of Personalized Medicine, Penn State College of Medicine, Hershey, Pennsylvania. Electronic address: dajiang.liu@psu.edu.

Scott Vrieze (S)

Department of Psychology, University of Minnesota, Minneapolis, Minnesota. Electronic address: vrieze@umn.edu.

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