Cluster Headache Genomewide Association Study and Meta-Analysis Identifies Eight Loci and Implicates Smoking as Causal Risk Factor.


Journal

Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449

Informations de publication

Date de publication:
10 2023
Historique:
revised: 22 06 2023
received: 01 03 2023
accepted: 07 07 2023
medline: 2 10 2023
pubmed: 24 7 2023
entrez: 24 7 2023
Statut: ppublish

Résumé

The objective of this study was to aggregate data for the first genomewide association study meta-analysis of cluster headache, to identify genetic risk variants, and gain biological insights. A total of 4,777 cases (3,348 men and 1,429 women) with clinically diagnosed cluster headache were recruited from 10 European and 1 East Asian cohorts. We first performed an inverse-variance genomewide association meta-analysis of 4,043 cases and 21,729 controls of European ancestry. In a secondary trans-ancestry meta-analysis, we included 734 cases and 9,846 controls of East Asian ancestry. Candidate causal genes were prioritized by 5 complementary methods: expression quantitative trait loci, transcriptome-wide association, fine-mapping of causal gene sets, genetically driven DNA methylation, and effects on protein structure. Gene set and tissue enrichment analyses, genetic correlation, genetic risk score analysis, and Mendelian randomization were part of the downstream analyses. The estimated single nucleotide polymorphism (SNP)-based heritability of cluster headache was 14.5%. We identified 9 independent signals in 7 genomewide significant loci in the primary meta-analysis, and one additional locus in the trans-ethnic meta-analysis. Five of the loci were previously known. The 20 genes prioritized as potentially causal for cluster headache showed enrichment to artery and brain tissue. Cluster headache was genetically correlated with cigarette smoking, risk-taking behavior, attention deficit hyperactivity disorder (ADHD), depression, and musculoskeletal pain. Mendelian randomization analysis indicated a causal effect of cigarette smoking intensity on cluster headache. Three of the identified loci were shared with migraine. This first genomewide association study meta-analysis gives clues to the biological basis of cluster headache and indicates that smoking is a causal risk factor. ANN NEUROL 2023;94:713-726.

Identifiants

pubmed: 37486023
doi: 10.1002/ana.26743
doi:

Types de publication

Meta-Analysis Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

713-726

Subventions

Organisme : Wellcome Trust
ID : 076113
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 085475
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 090355
Pays : United Kingdom

Informations de copyright

© 2023 The Authors. Annals of Neurology published by Wiley Periodicals LLC on behalf of American Neurological Association.

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Auteurs

Bendik S Winsvold (BS)

Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Department of Neurology, Oslo University Hospital, Oslo, Norway.
Norwegian Centre for Headache Research (NorHEAD), Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.

Aster V E Harder (AVE)

Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.
Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands.

Caroline Ran (C)

Centre for Cluster Headache, Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Mona A Chalmer (MA)

Department of Neurology, Danish Headache Center, Rigshospitalet-Glostrup, University of Copenhagen University Hospital, Glostrup, Denmark.

Maria Carolina Dalmasso (MC)

Division of Neurogenetics and Molecular Psychiatry, Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Neurosciences and Complex Systems Unit (EnyS), CONICET, Hospital El Cruce 'N. Kirchner', National University A. Jauretche (UNAJ), Florencio Varela, Argentina.

Egil Ferkingstad (E)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.

Kumar Parijat Tripathi (KP)

Division of Neurogenetics and Molecular Psychiatry, Department of Psychiatry, Uniklinik Köln, Cologne, Germany.

Elena Bacchelli (E)

Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy.

Sigrid Børte (S)

Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Norwegian Centre for Headache Research (NorHEAD), Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.

Carmen Fourier (C)

Centre for Cluster Headache, Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Anja S Petersen (AS)

Department of Neurology, Danish Headache Center, Rigshospitalet-Glostrup, University of Copenhagen University Hospital, Glostrup, Denmark.

Lisanne S Vijfhuizen (LS)

Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.

Sigurdur H Magnusson (SH)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.

Emer O'Connor (E)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Gyda Bjornsdottir (G)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.

Paavo Häppölä (P)

Institute for Molecular Medicine Finland (FIMM), Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Helsinki, Finland.

Yen-Feng Wang (YF)

Department of Neurology, Taipei Veterans General Hospital, Taipei, Taiwan.
Brain Research Center, National Yang Ming Chiao Tung University, Taipei, Taiwan.

Ida Callesen (I)

Department of Neurology, Danish Headache Center, Rigshospitalet-Glostrup, University of Copenhagen University Hospital, Glostrup, Denmark.

Tim Kelderman (T)

Department of Neurology, Ghent University Hospital, Ghent, Belgium.

Victor J Gallardo (VJ)

Headache and Neurological Pain Research Group, Vall d'Hebron Research Institute, Departament de Medicina, Universitat Autònoma de Barcelona, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.

Irene de Boer (I)

Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands.

Felicia Jennysdotter Olofsgård (FJ)

Centre for Cluster Headache, Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Katja Heinze (K)

Kiel Migraine and Headache Centre, Kiel, Germany.

Nunu Lund (N)

Department of Neurology, Danish Headache Center, Rigshospitalet-Glostrup, University of Copenhagen University Hospital, Glostrup, Denmark.

Laurent F Thomas (LF)

K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
BioCore-Bioinformatics Core Facility, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Clinic of Laboratory Medicine, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway.

Chia-Lin Hsu (CL)

Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.

Matti Pirinen (M)

Institute for Molecular Medicine Finland (FIMM), Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Helsinki, Finland.
Department of Public Health, University of Helsinki, Helsinki, Finland.
Department of Mathematics and Statistics, University of Helsinki, Helsinki, Finland.

Heidi Hautakangas (H)

Institute for Molecular Medicine Finland (FIMM), Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Helsinki, Finland.

Marta Ribasés (M)

Psychiatric Genetics Unit, Group of Psychiatry, Mental Health and Addiction, Universitat Autònoma de Barcelona, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.
Department of Psychiatry, Vall d'Hebron University Hospital, Barcelona, Spain.
Biomedical Network Research Centre on Mental Health (CIBERSAM), Instituto de Salud Carlos III, Madrid, Spain.
Department of Genetics, Microbiology, and Statistics, Faculty of Biology, Universitat de Barcelona, Barcelona, Spain.

Simona Guerzoni (S)

AOU Policlinico Modena, Modena University Hospital, Modena, Italy.

Prasanth Sivakumar (P)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Janice Yip (J)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Axel Heinze (A)

Kiel Migraine and Headache Centre, Kiel, Germany.

Fahri Küçükali (F)

Complex Genetics of Alzheimer's Disease Group, Center for Molecular Neurology, VIB, Antwerp, Belgium.
Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Sisse R Ostrowski (SR)

Department of Clinical Immunology, Centre of Diagnostic Investigation, Rigshospitalet, Copenhagen, Denmark.
Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.

Ole B Pedersen (OB)

Department of Clinical Immunology, Zealand University Hospital, Køge, Denmark.

Espen S Kristoffersen (ES)

Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
Norwegian Centre for Headache Research (NorHEAD), Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Department of General Practice, University of Oslo, Oslo, Norway.
Department of Neurology, Akershus University Hospital, Lørenskog, Norway.

Amy E Martinsen (AE)

Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Norwegian Centre for Headache Research (NorHEAD), Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway.

María S Artigas (MS)

Psychiatric Genetics Unit, Group of Psychiatry, Mental Health and Addiction, Universitat Autònoma de Barcelona, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.
Department of Psychiatry, Vall d'Hebron University Hospital, Barcelona, Spain.
Biomedical Network Research Centre on Mental Health (CIBERSAM), Instituto de Salud Carlos III, Madrid, Spain.
Department of Genetics, Microbiology, and Statistics, Faculty of Biology, Universitat de Barcelona, Barcelona, Spain.

Susie Lagrata (S)

Headache and Facial Pain Group, University College London Queen Square Institute of Neurology and National Hospital for Neurology and Neurosurgery, London, UK.

Maria Michela Cainazzo (MM)

AOU Policlinico Modena, Modena University Hospital, Modena, Italy.

Joycee Adebimpe (J)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Olivia Quinn (O)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Carl Göbel (C)

Kiel Migraine and Headache Centre, Kiel, Germany.
Department of Neurology, University Hospital Schleswig-Holstein, Lübeck, Germany.

Anna Cirkel (A)

Kiel Migraine and Headache Centre, Kiel, Germany.
Department of Neurology, University Hospital Schleswig-Holstein, Lübeck, Germany.

Alexander E Volk (AE)

Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Stefanie Heilmann-Heimbach (S)

Institute of Human Genetics, University of Bonn, School of Medicine & University Hospital Bonn, Bonn, Germany.

Anne Heidi Skogholt (AH)

K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.

Maiken E Gabrielsen (ME)

K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.

Leopoldine A Wilbrink (LA)

Department of Neurology, Zuyderland Hospital, Heerlen, The Netherlands.

Daisuke Danno (D)

Headache and Facial Pain Group, University College London Queen Square Institute of Neurology and National Hospital for Neurology and Neurosurgery, London, UK.

Dwij Mehta (D)

Headache and Facial Pain Group, University College London Queen Square Institute of Neurology and National Hospital for Neurology and Neurosurgery, London, UK.

Daníel F Guðbjartsson (DF)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.

Frits R Rosendaal (FR)

Department of Clinical Epidemiology, Leiden University Medical Center, Leiden, The Netherlands.

Ko Willems van Dijk (K)

Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.
Einthoven Laboratory for Experimental Vascular Medicine, Leiden University Medical Center, Leiden, The Netherlands.
Department of Internal Medicine, Division of Endocrinology, Leiden University Medical Center, Leiden, The Netherlands.

Rolf Fronczek (R)

Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands.

Michael Wagner (M)

Department of Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Bonn, Germany.
German Center for Neurodegenerative Diseases (DZNE Bonn), Bonn, Germany.

Martin Scherer (M)

Department of Primary Medical Care, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Hartmut Göbel (H)

Kiel Migraine and Headache Centre, Kiel, Germany.

Kristel Sleegers (K)

Complex Genetics of Alzheimer's Disease Group, Center for Molecular Neurology, VIB, Antwerp, Belgium.
Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Olafur A Sveinsson (OA)

Faculty of Medicine, School of Health Sciences, University of Iceland, Reykjavik, Iceland.

Luca Pani (L)

Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy.
Department of Psychiatry and Behavioral Sciences, University of Miami, Miami, FL.

Michele Zoli (M)

Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy.

Josep A Ramos-Quiroga (JA)

Psychiatric Genetics Unit, Group of Psychiatry, Mental Health and Addiction, Universitat Autònoma de Barcelona, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.
Department of Psychiatry, Vall d'Hebron University Hospital, Barcelona, Spain.
Biomedical Network Research Centre on Mental Health (CIBERSAM), Instituto de Salud Carlos III, Madrid, Spain.
Department of Psychiatry and Forensic Medicine, Universitat Autònoma de Barcelona, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.

Efthimios Dardiotis (E)

Department of Neurology, Faculty of Medicine, University of Thessaly, Volos, Greece.

Anna Steinberg (A)

Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
Department of Neurology, Karolinska University Hospital, Stockholm, Sweden.

Steffi Riedel-Heller (S)

Institute of Social Medicine, Occupational Health and Public Health, University of Leipzig, Leipzig, Germany.

Christina Sjöstrand (C)

Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
Department of Neurology, Danderyd Hospital, Stockholm, Sweden.

Thorgeir E Thorgeirsson (TE)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.

Hreinn Stefansson (H)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.

Laura Southgate (L)

Molecular and Clinical Sciences Research Institute, St. George's, University of London, London, UK.
Department of Medical & Molecular Genetics, Faculty of Life Sciences & Medicine, King's College London, London, UK.

Richard C Trembath (RC)

Department of Medical & Molecular Genetics, Faculty of Life Sciences & Medicine, King's College London, London, UK.

Jana Vandrovcova (J)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Raymond Noordam (R)

Department of Internal Medicine, Section of Gerontology and Geriatrics, Leiden University Medical Center, Leiden, The Netherlands.

Koen Paemeleire (K)

Department of Neurology, Ghent University Hospital, Ghent, Belgium.

Kari Stefansson (K)

deCODE genetics/Amgen Inc., Reykjavik, Iceland.
Faculty of Medicine, School of Health Sciences, University of Iceland, Reykjavik, Iceland.

Cathy Shen-Jang Fann (CS)

Institute of Biomedical Sciences, Academia Sinica, Taipei, Taiwan.

Elisabet Waldenlind (E)

Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.
Department of Neurology, Karolinska University Hospital, Stockholm, Sweden.

Erling Tronvik (E)

Norwegian Centre for Headache Research (NorHEAD), Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Department of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Department of Neurology and Clinical Neurophysiology, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway.

Rigmor H Jensen (RH)

Department of Neurology, Danish Headache Center, Rigshospitalet-Glostrup, University of Copenhagen University Hospital, Glostrup, Denmark.

Shih-Pin Chen (SP)

Brain Research Center, National Yang Ming Chiao Tung University, Taipei, Taiwan.
Department of Medical Research, Division of Translational Research, Taipei Veterans General Hospital, Taipei, Taiwan.

Henry Houlden (H)

Department of Neuromuscular Diseases, Institute of Neurology, University College London, London, UK.

Gisela M Terwindt (GM)

Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands.

Christian Kubisch (C)

Institute of Human Genetics, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Elena Maestrini (E)

Department of Pharmacy and Biotechnology, University of Bologna, Bologna, Italy.

Michail Vikelis (M)

Glyfada Headache Center, Glyfada, Greece.

Patricia Pozo-Rosich (P)

Headache and Neurological Pain Research Group, Vall d'Hebron Research Institute, Departament de Medicina, Universitat Autònoma de Barcelona, Vall d'Hebron Research Institute (VHIR), Barcelona, Spain.
Headache Unit, Neurology Department, Vall d'Hebron University Hospital, Barcelona, Spain.

Andrea C Belin (AC)

Centre for Cluster Headache, Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Manjit Matharu (M)

Headache and Facial Pain Group, University College London Queen Square Institute of Neurology and National Hospital for Neurology and Neurosurgery, London, UK.

Arn M J M van den Maagdenberg (AMJM)

Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands.
Department of Neurology, Leiden University Medical Center, Leiden, The Netherlands.

Thomas F Hansen (TF)

Department of Neurology, Danish Headache Center, Rigshospitalet-Glostrup, University of Copenhagen University Hospital, Glostrup, Denmark.
Novo Nordic Foundation Center for Protein Research, University of Copenhagen, Copenhagen, Denmark.

Alfredo Ramirez (A)

Division of Neurogenetics and Molecular Psychiatry, Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, University of Cologne, Cologne, Germany.
Department of Neurodegenerative Diseases and Geriatric Psychiatry, University Hospital Bonn, Bonn, Germany.
German Center for Neurodegenerative Diseases (DZNE Bonn), Bonn, Germany.
Glenn Biggs Institute for Alzheimer's & Neurodegenerative Diseases, University of Texas Health Sciences Center, San Antonio, TX.
Cluster of Excellence Cellular Stress Responses in Aging-associated Diseases (CECAD), University of Cologne, Cologne, Germany.

John-Anker Zwart (JA)

Department of Research and Innovation, Division of Clinical Neuroscience, Oslo University Hospital, Oslo, Norway.
K. G. Jebsen Center for Genetic Epidemiology, Department of Public Health and Nursing, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Norwegian Centre for Headache Research (NorHEAD), Department of Neuromedicine and Movement Science, Norwegian University of Science and Technology (NTNU), Trondheim, Norway.
Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway.

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