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PMID: 25064009 Published · ppublish English Journal Article Meta-Analysis Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson's disease.

Nature genetics ·Vol. 46 ·No. 9 ·2014-09-00 ·Pages 989-93

Nalls MA, Pankratz N, Lill CM, Do CB, Hernandez DG, Saad M, DeStefano AL, Kara E, Bras J, Sharma M, Schulte C, Keller MF, Arepalli S, Letson C, Edsall C, Stefansson H, Liu X, Pliner H, Lee JH, Cheng R, International Parkinson's Disease Genomics Consortium IPDGC, Parkinson's Study Group PSG Parkinson's Research: The Organized GENetics Initiative PROGENI, 23andMe, GenePD, NeuroGenetics Research Consortium NGRC, Hussman Institute of Human Genomics HIHG, Ashkenazi Jewish Dataset Investigator, Cohorts for Health and Aging Research in Genetic Epidemiology CHARGE, North American Brain Expression Consortium NABEC, United Kingdom Brain Expression Consortium UKBEC, Greek Parkinson's Disease Consortium, Alzheimer Genetic Analysis Group, Ikram MA, Ioannidis JP, Hadjigeorgiou GM, Bis JC, Martinez M, Perlmutter JS, Goate A, Marder K, Fiske B, Sutherland M, Xiromerisiou G, Myers RH, Clark LN, Stefansson K, Hardy JA, Heutink P, Chen H, Wood NW, Houlden H, Payami H, Brice A, Scott WK, Gasser T, Bertram L, Eriksson N, Foroud T, Singleton AB

Abstract

We conducted a meta-analysis of Parkinson's disease genome-wide association studies using a common set of 7,893,274 variants across 13,708 cases and 95,282 controls. Twenty-six loci were identified as having genome-wide significant association; these and 6 additional previously reported loci were then tested in an independent set of 5,353 cases and 5,551 controls. Of the 32 tested SNPs, 24 replicated, including 6 newly identified loci. Conditional analyses within loci showed that four loci, including GBA, GAK-DGKQ, SNCA and the HLA region, contain a secondary independent risk variant. In total, we identified and replicated 28 independent risk variants for Parkinson's disease across 24 loci. Although the effect of each individual locus was small, risk profile analysis showed substantial cumulative risk in a comparison of the highest and lowest quintiles of genetic risk (odds ratio (OR) = 3.31, 95% confidence interval (CI) = 2.55-4.30; P = 2 × 10(-16)). We also show six risk loci associated with proximal gene expression or DNA methylation.

MeSH Terms

Case-Control Studies Genetic Loci Genetic Predisposition to Disease Genome-Wide Association Study/methods Genotype Humans Parkinson Disease/genetics Polymorphism, Single Nucleotide Risk Factors

Authors & Affiliations

59 authors, click to expand affiliations / ORCID

Nalls Mike A

1] Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA. [2].

Pankratz Nathan

1] Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, Minnesota, USA. [2].

Lill Christina M

1] Department of Vertebrate Genomics, Max Planck Institute for Molecular Genetics, Berlin, Germany. [2] Department of Neurology, Focus Program Translational Neuroscience, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany.

Do Chuong B

23andMe, Inc., Mountain View, California, USA.

Hernandez Dena G

1] Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA. [2] Reta Lila Weston Institute, University College London Institute of Neurology, Queen Square, London, UK.

Saad Mohamad

1] Department of Biostatistics, University of Washington, Seattle, Washington, USA. [2] INSERM, UMR 1043, Centre de Physiopathologie de Toulouse-Purpan, Toulouse, France. [3] Paul Sabatier University, Toulouse, France.

DeStefano Anita L

1] Department of Neurology, Boston University School of Medicine, Boston, Massachusetts, USA. [2] Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts, USA. [3] National Heart, Lung, and Blood Institute (NHLBI) Framingham Heart Study, Framingham, Massachusetts, USA.

Kara Eleanna

Department of Molecular Neuroscience, Institute of Neurology, University College London, London, UK.

Bras Jose

Department of Molecular Neuroscience, Institute of Neurology, University College London, London, UK.

Sharma Manu

1] Institute for Clinical Epidemiology and Applied Biometry, University of Tübingen, Tübingen, Germany. [2] Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Schulte Claudia

Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Keller Margaux F

Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA.

Arepalli Sampath

Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA.

Letson Christopher

Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA.

Edsall Connor

Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA.

Stefansson Hreinn

deCODE Genetics, Reykjavík, Iceland.

Liu Xinmin

Department of Pathology and Cell Biology, Columbia University Medical Center, New York, New York, USA.

Pliner Hannah

Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA.

Lee Joseph H

The Taub Institute for Alzheimer's Disease and the Aging Brain, Columbia University Medical Center, New York, New York, USA.

Cheng Rong

The Taub Institute for Alzheimer's Disease and the Aging Brain, Columbia University Medical Center, New York, New York, USA.

International Parkinson's Disease Genomics Consortium (IPDGC)

Parkinson's Study Group (PSG) Parkinson's Research: The Organized GENetics Initiative (PROGENI)

23andMe

GenePD

NeuroGenetics Research Consortium (NGRC)

Hussman Institute of Human Genomics (HIHG)

Ashkenazi Jewish Dataset Investigator

Cohorts for Health and Aging Research in Genetic Epidemiology (CHARGE)

North American Brain Expression Consortium (NABEC)

United Kingdom Brain Expression Consortium (UKBEC)

Greek Parkinson's Disease Consortium

Alzheimer Genetic Analysis Group

Ikram M Arfan

1] Department of Epidemiology, Erasmus MC University Medical Center, Rotterdam, the Netherlands. [2] Department of Radiology, Erasmus MC University Medical Center, Rotterdam, the Netherlands. [3] Department of Neurology, Erasmus MC University Medical Center, Rotterdam, the Netherlands.

Ioannidis John P A

Stanford Prevention Research Center, Stanford University, Stanford, California, USA.

Hadjigeorgiou Georgios M

Neuroscience Unit, Department of Neurology, Faculty of Medicine, University of Thessaly, Larissa, Greece.

Bis Joshua C

Cardiovascular Health Research Unit, Department of Medicine, University of Washington, Seattle, Washington, USA.

Martinez Maria

1] INSERM, UMR 1043, Centre de Physiopathologie de Toulouse-Purpan, Toulouse, France. [2] Paul Sabatier University, Toulouse, France.

Perlmutter Joel S

1] Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, Missouri, USA. [2] Department of Radiology, Washington University School of Medicine, St. Louis, Missouri, USA. [3] Department of Neurology, Washington University School of Medicine, St. Louis, Missouri, USA.

Goate Alison

1] Hope Center for Neurological Disorders, Washington University School of Medicine, St. Louis, Missouri, USA. [2] Department of Neurology, Washington University School of Medicine, St. Louis, Missouri, USA. [3] Department of Psychiatry, Washington University School of Medicine, St. Louis, Missouri, USA. [4] Department of Genetics, Washington University School of Medicine, St. Louis, Missouri, USA.

Marder Karen

1] The Taub Institute for Alzheimer's Disease and the Aging Brain, Columbia University Medical Center, New York, New York, USA. [2] Gertrude H. Sergievsky Center, Columbia University Medical Center, New York, New York, USA. [3] Department of Neurology, Columbia University Medical Center, New York, New York, USA. [4] Department of Psychiatry, Columbia University Medical Center, New York, New York, USA.

Fiske Brian

The Michael J. Fox Foundation for Parkinson's Research, New York, New York, USA.

Sutherland Margaret

Neuroscience Center, National Institute of Neurological Disorders and Stroke, Bethesda, Maryland, USA.

Xiromerisiou Georgia

1] Neuroscience Unit, Department of Neurology, Faculty of Medicine, University of Thessaly, Larissa, Greece. [2] Department of Neurology, Papageorgiou Hospital, Thessaloniki, Greece.

Myers Richard H

Department of Neurology, Boston University School of Medicine, Boston, Massachusetts, USA.

Clark Lorraine N

1] Department of Pathology and Cell Biology, Columbia University Medical Center, New York, New York, USA. [2] The Taub Institute for Alzheimer's Disease and the Aging Brain, Columbia University Medical Center, New York, New York, USA.

Stefansson Kari

deCODE Genetics, Reykjavík, Iceland.

Hardy John A

Reta Lila Weston Institute, University College London Institute of Neurology, Queen Square, London, UK.

Heutink Peter

Genome Biology for Neurodegenerative Diseases, German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.

Chen Honglei

Epidemiology Branch, National Institute of Environmental Health Sciences, US National Institutes of Health, Research Triangle, North Carolina, USA.

Wood Nicholas W

Department of Molecular Neuroscience, Institute of Neurology, University College London, London, UK.

Houlden Henry

Department of Molecular Neuroscience, Institute of Neurology, University College London, London, UK.

Payami Haydeh

New York State Department of Health Wadsworth Center, Albany, New York, USA.

Brice Alexis

1] Sorbonne Université, UPMC Université Paris 06, UM 75, INSERM U1127, Institut du Cerveau et de la Moelle, Paris, France. [2] CNRS, UMR 7225, Paris, France. [3] Pitié-Salpêtrière Hospital, Department of Genetics and Cytogenetics, Paris, France.

Scott William K

Department of Human Genetics, University of Miami School of Medicine, Miami, Florida, USA.

Gasser Thomas

Department for Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Bertram Lars

1] Department of Vertebrate Genomics, Max Planck Institute for Molecular Genetics, Berlin, Germany. [2] School of Public Health, Faculty of Medicine, The Imperial College of Science, Technology and Medicine, London, UK.

Eriksson Nicholas

23andMe, Inc., Mountain View, California, USA.

Foroud Tatiana

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

Singleton Andrew B

Laboratory of Neurogenetics, National Institute on Aging, Bethesda, Maryland, USA.

Investigators

471 investigators, click to expand

Nalls Mike A

Plagnol Vincent

Hernandez Dena G

Sharma Manu

Sheerin Una-Marie

Saad Mohamad

Simón-Sánchez Javier

Schulte Claudia

Lesage Suzanne

Sveinbjörnsdóttir Sigurlaug

Arepalli Sampath

Barker Roger

Ben-Shlomo Yoav

Berendse Henk W

Berg Daniela

Bhatia Kailash

de Bie Rob M A

Biffi Alessandro

Bloem Bas

Bochdanovits Zoltan

Bonin Michael

Bras Jose M

Brockmann Kathrin

Brooks Janet

Burn David J

Charlesworth Gavin

Chen Honglei

Chinnery Patrick F

Chong Sean

Clarke Carl E

Cookson Mark R

Cooper J Mark

Corvol Jean Christophe

Counsell Carl

Damier Philippe

Dartigues Jean-François

Deloukas Panos

Deuschl Günther

Dexter David T

van Dijk Karin D

Dillman Allissa

Durif Frank

Dürr Alexandra

Edkins Sarah

Evans Jonathan R

Foltynie Thomas

Dong Jing

Gardner Michelle

Gibbs J Raphael

Goate Alison

Gray Emma

Guerreiro Rita

Harris Clare

van Hilten Jacobus J

Hofman Albert

Hollenbeck Albert

Holton Janice

Hu Michele

Huang Xuemei

Wurster Isabel

Mätzler Walter

Hudson Gavin

Hunt Sarah E

Huttenlocher Johanna

Illig Thomas

Jónsson Pálmi V

Lambert Jean-Charles

Langford Cordelia

Lees Andrew

Lichtner Peter

Limousin Patricia

Lopez Grisel

Lorenz Delia

McNeill Alisdair

Moorby Catriona

Moore Matthew

Morris Huw R

Morrison Karen E

Mudanohwo Ese

O'Sullivan Sean S

Pearson Justin

Perlmutter Joel S

Pétursson Hjörvar

Pollak Pierre

Post Bart

Potter Simon

Ravina Bernard

Revesz Tamas

Riess Olaf

Rivadeneira Fernando

Rizzu Patrizia

Ryten Mina

Sawcer Stephen

Schapira Anthony

Scheffer Hans

Shaw Karen

Shoulson Ira

Sidransky Ellen

Smith Colin

Spencer Chris C A

Stefánsson Hreinn

Bettella Francesco

Stockton Joanna D

Strange Amy

Talbot Kevin

Tanner Carlie M

Tashakkori-Ghanbaria Avazeh

Tison François

Trabzuni Daniah

Traynor Bryan J

Uitterlinden André G

Velseboer Daan

Vidailhet Marie

Walker Robert

van de Warrenburg Bart

Wickremaratchi Mirdhu

Williams Nigel

Williams-Gray Caroline H

Winder-Rhodes Sophie

Stefánsson Kári

Martinez Maria

Wood Nicholas W

Hardy John

Heutink Peter

Brice Alexis

Gasser Thomas

Singleton Andrew B

Factor S

Higgins D

Evans S

Shill H

Stacy M

Danielson J

Marlor L

Williamson K

Jankovic J

Hunter C

Simon D

Ryan P

Scollins L

Saunders-Pullman R

Boyar K

Costan-Toth C

Ohmann E

Sudarsky L

Joubert C

Friedman J

Chou K

Fernandez H

Lannon M

Galvez-Jimenez N

Podichetty A

Thompson K

Lewitt P

DeAngelis M

O'Brien C

Seeberger L

Dingmann C

Judd D

Marder K

Fraser J

Harris J

Bertoni J

Peterson C

Rezak M

Medalle G

Chouinard S

Panisset M

Hall J

Poiffaut H

Calabrese V

Roberge P

Wojcieszek J

Belden J

Jennings D

Marek K

Mendick S

Reich S

Dunlop B

Jog M

Horn C

Uitti R

Turk M

Ajax T

Mannetter J

Sethi K

Carpenter J

Dill B

Hatch L

Ligon K

Narayan S

Blindauer K

Abou-Samra K

Petit J

Elmer L

Aiken E

Davis K

Schell C

Wilson S

Velickovic M

Koller W

Phipps S

Feigin A

Gordon M

Hamann J

Licari E

Marotta-Kollarus M

Shannon B

Winnick R

Simuni T

Videnovic A

Kaczmarek A

Williams K

Wolff M

Rao J

Cook M

Fernandez M

Kostyk S

Hubble J

Campbell A

Reider C

Seward A

Camicioli R

Carter J

Nutt J

Andrews P

Morehouse S

Stone C

Mendis T

Grimes D

Alcorn-Costa C

Gray P

Haas K

Vendette J

Sutton J

Hutchinson B

Young J

Rajput A

Klassen L

Shirley T

Manyam B

Simpson P

Whetteckey J

Wulbrecht B

Truong D

Pathak M

Frei K

Luong N

Tra T

Tran A

Vo J

Lang A

Kleiner- Fisman G

Nieves A

Johnston L

So J

Podskalny G

Giffin L

Atchison P

Allen C

Martin W

Wieler M

Suchowersky O

Furtado S

Klimek M

Hermanowicz N

Niswonger S

Shults C

Fontaine D

Aminoff M

Christine C

Diminno M

Hevezi J

Dalvi A

Kang U

Richman J

Uy S

Young J

Dalvi A

Sahay A

Gartner M

Schwieterman D

Hall D

Leehey M

Culver S

Derian T

Demarcaida T

Thurlow S

Rodnitzky R

Dobson J

Lyons K

Pahwa R

Gales T

Thomas S

Shulman L

Reich S

Weiner W

Dustin K

Lyons K

Singer C

Koller W

Weiner W

Zelaya L

Tuite P

Hagen V

Rolandelli S

Schacherer R

Kosowicz J

Gordon P

Werner J

Serrano C

Roque S

Kurlan R

Berry D

Gardiner I

Hauser R

Sanchez-Ramos J

Zesiewicz T

Delgado H

Price K

Rodriguez P

Wolfrath S

Pfeiffer R

Davis L

Pfeiffer B

Dewey R

Hayward B

Johnson A

Meacham M

Estes B

Walker F

Hunt V

O'Neill C

Racette B

Swisher L

Dijamco Cheri

Conley Emily Drabant

Dorfman Elizabeth

Tung Joyce Y

Hinds David A

Mountain Joanna L

Wojcicki Anne

Lew M

Suchowersky O

Klein C

Golbe L

Growdon J

Wooten G F

Watts R

Guttman M

Racette B

Marlor L

Shill H

Singer C

Goldwurm S

Saint-Hilaire M H

Baker K

Litvan I

Nicholson G

Nance M

Drasby E

Isaacson S

Burn D

Pramstaller P

Al-hinti J

Moller A

Sherman S

Roxburgh R

Slevin J

Perlmutter J

Mark M H

Huggins N

Pezzoli G

Massood T

Itin I

Corbett A

Chinnery P

Ostergaard K

Snow B

Cambi F

Kay D

Samii A

Nutt J

Agarwal P

Roberts J W

Higgins D S

Molho Eric

Rosen Ami

Montimurro J

Martinez E

Griffith A

Kusel V

Yearout D

Factor S

Zabetian C

Clark L N

Liu X

Lee J H

Taub R Cheng

Marder K

Louis E D

Cote L J

Waters C

Ford B

Fahn S

Vance Jeffery M

Beecham Gary W

Martin Eden R

Nuytemans Karen

Pericak-Vance Margaret A

Haines Jonathan L

DeStefano Anita

Seshadri Sudha

Choi Seung Hoan

Frank Samuel

Bis Joshua C

Psaty Bruce M

Rice Kenneth

Longstreth W T

Ton Thanh G N

Jain Samay

Ikram M Arfan

van Duijn Cornelia M

Hofman Albert

Uitterlinden André G

Verlinden Vincent J

Koudstaal Peter J

Singleton Andrew

Cookson Mark

Gibbs J Raphael

Hernandez Dena

Dillman Allissa

Nalls Michael

Zonderman Alan

Arepalli Sampath

Ferrucci Luigi

Johnson Robert

Longo Dan

O'Brien Richard

Traynor Bryan

Troncoso Juan

van der Brug Marcel

Zielke Ronald

Hardy John

Weale Michael

Ryten Mina

Ramasamy Adaikalavan

Trabzuni Daniah

Smith Colin

Walker Robert

Kara Eleanna

Xiromerisiou Georgia

Dardiotis Efthimios

Tsimourtou Vana

Spanaki Cleanthe

Plaitakis Andreas

Bozi Maria

Stefanis Leonidas

Vassilatis Dimitris

Koutsis Georgios

Panas Marios

Houlden Henry

Hadjigeorgiou Georgios M

Guerreiro Rita

Lunnon Katie

Lupton Michelle

Powell John

Parkkinen Laura

Ansorge Olaf

Hardy John

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Article Info

Journal

Nature genetics

Abbr.

Nat Genet

ISSN

1546-1718

DOI

10.1038/ng.3043

Published

2014-09-00

Epub

2014-00-27

Pages

989-93

Language

English

Region

United States

NLM ID

9216904

PMCID

PMC4146673

Subset

Grants

Medical Research Council · G0901254 · United Kingdom

Parkinson's UK · J-0804 · United Kingdom

Medical Research Council · G0701075 · United Kingdom

Medical Research Council · G1100643 · United Kingdom

Medical Research Council · MR/L016400/1 · United Kingdom

Wellcome Trust · WT089698/Z/09/Z · United Kingdom

Parkinson's UK · G-0909 · United Kingdom

NINDS NIH HHS · NS036630 · United States

Medical Research Council · G0802760 · United Kingdom

NCI NIH HHS · R01CA141668 · United States

NIA NIH HHS · AG025259 · United States

Medical Research Council · G0802462 · United Kingdom

NCATS NIH HHS · UL1TR000124 · United States

NINDS NIH HHS · NS060113 · United States

Intramural NIH HHS · Z01 AG000949-03 · United States

NINDS NIH HHS · NS050487 · United States

NHLBI NIH HHS · R01 HL120393 · United States

NINDS NIH HHS · U01 NS082151 · United States

Parkinson's UK · G-0907 · United Kingdom

NIA NIH HHS · U24 AG021886 · United States

Parkinson's UK · F-1202 · United Kingdom

Wellcome Trust · 083948/Z/07/Z · United Kingdom

NINDS NIH HHS · 1K23NS070867 · United States

Medical Research Council · MC_G0901330 · United Kingdom

Medical Research Council · G1001253 · United Kingdom

Medical Research Council · G0700943 · United Kingdom

NIA NIH HHS · U24 AG056270 · United States

NIA NIH HHS · AG033193 · United States

Wellcome Trust · 076113 · United Kingdom

NCATS NIH HHS · UL1 TR000124 · United States

Medical Research Council · G108/638 · United Kingdom

Medical Research Council · MC_G1000735 · United Kingdom

NINDS NIH HHS · R01 NS075321 · United States

NINDS NIH HHS · NS17950 · United States

NCATS NIH HHS · UL1 TR001108 · United States

NINDS NIH HHS · K02 NS073836 · United States

Medical Research Council · MR/L501554/1 · United Kingdom

NIA NIH HHS · AG08122 · United States

Wellcome Trust · 089698 · United Kingdom

NINDS NIH HHS · R01 NS088538 · United States

Intramural NIH HHS · Z01 AG000932-01 · United States

NIA NIH HHS · P30AG013846 · United States

NINDS NIH HHS · R01NS037167 · United States

NCRR NIH HHS · 1KL2RR024154 · United States

NCRR NIH HHS · 2UL1 RR024156 · United States

NIA NIH HHS · R01 AG041797 · United States

Medical Research Council · MR/J004758/1 · United Kingdom

NIA NIH HHS · AG031287 · United States

Medical Research Council · G1100479 · United Kingdom

NIA NIH HHS · P30AG024826 · United States

NINDS NIH HHS · P50 NS038377 · United States

NIDDK NIH HHS · DK063491 · United States

NIA NIH HHS · AG16495 · United States

Wellcome Trust · 085475 · United Kingdom

Wellcome Trust · 090355 · United Kingdom

NINDS NIH HHS · R01-NS-36960 · United States

Medical Research Council · MR/L010305/1 · United Kingdom

NHGRI NIH HHS · R44 HG006981 · United States

NIA NIH HHS · AG023629 · United States

Medical Research Council · MC_PC_09003 · United Kingdom

NINDS NIH HHS · P50 NS071674 · United States

NINDS NIH HHS · R01 NS076843 · United States

NINDS NIH HHS · P50NS071674 · United States

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PubMed source DOI: 10.1038/ng.3043 PMC Full Text View journal details

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Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson's disease.

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