Shared Genetics of Multiple System Atrophy and Inflammatory Bowel Disease.


Journal

Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688

Informations de publication

Date de publication:
02 2021
Historique:
received: 09 04 2020
revised: 01 09 2020
accepted: 21 09 2020
pubmed: 28 10 2020
medline: 28 4 2021
entrez: 27 10 2020
Statut: ppublish

Résumé

Multiple system atrophy (MSA) is a rare neurodegenerative disease characterized by intracellular accumulations of α-synuclein and nerve cell loss in striatonigral and olivopontocerebellar structures. Epidemiological and clinical studies have reported potential involvement of autoimmune mechanisms in MSA pathogenesis. However, genetic etiology of this interaction remains unknown. We aimed to investigate genetic overlap between MSA and 7 autoimmune diseases and to identify shared genetic loci. Genome-wide association study summary statistics of MSA and 7 autoimmune diseases were combined in cross-trait conjunctional false discovery rate analysis to explore overlapping genetic background. Expression of selected candidate genes was compared in transgenic MSA mice and wild-type mice. Genetic variability of candidate genes was further investigated using independent whole-exome genotyping data from large cohorts of MSA and autoimmune disease patients and healthy controls. We observed substantial polygenic overlap between MSA and inflammatory bowel disease and identified 3 shared genetic loci with leading variants upstream of the DENND1B and RSP04 genes, and in intron of the C7 gene. Further, the C7 gene showed significantly dysregulated expression in the degenerating midbrain of transgenic MSA mice compared with wild-type mice and had elevated burden of protein-coding variants in independent MSA and inflammatory bowel disease cohorts. Our study provides evidence of shared genetic etiology between MSA and inflammatory bowel disease with an important role of the C7 gene in both phenotypes, with the implication of immune and gut dysfunction in MSA pathophysiology. © 2020 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Sections du résumé

BACKGROUND
Multiple system atrophy (MSA) is a rare neurodegenerative disease characterized by intracellular accumulations of α-synuclein and nerve cell loss in striatonigral and olivopontocerebellar structures. Epidemiological and clinical studies have reported potential involvement of autoimmune mechanisms in MSA pathogenesis. However, genetic etiology of this interaction remains unknown. We aimed to investigate genetic overlap between MSA and 7 autoimmune diseases and to identify shared genetic loci.
METHODS
Genome-wide association study summary statistics of MSA and 7 autoimmune diseases were combined in cross-trait conjunctional false discovery rate analysis to explore overlapping genetic background. Expression of selected candidate genes was compared in transgenic MSA mice and wild-type mice. Genetic variability of candidate genes was further investigated using independent whole-exome genotyping data from large cohorts of MSA and autoimmune disease patients and healthy controls.
RESULTS
We observed substantial polygenic overlap between MSA and inflammatory bowel disease and identified 3 shared genetic loci with leading variants upstream of the DENND1B and RSP04 genes, and in intron of the C7 gene. Further, the C7 gene showed significantly dysregulated expression in the degenerating midbrain of transgenic MSA mice compared with wild-type mice and had elevated burden of protein-coding variants in independent MSA and inflammatory bowel disease cohorts.
CONCLUSION
Our study provides evidence of shared genetic etiology between MSA and inflammatory bowel disease with an important role of the C7 gene in both phenotypes, with the implication of immune and gut dysfunction in MSA pathophysiology. © 2020 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 33107653
doi: 10.1002/mds.28338
pmc: PMC8985479
mid: NIHMS1789384
doi:

Substances chimiques

alpha-Synuclein 0

Types de publication

Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

449-459

Subventions

Organisme : Wellcome Trust
ID : 202903/Z/16/Z
Pays : United Kingdom
Organisme : Intramural NIH HHS
ID : Z01 AG000949
Pays : United States
Organisme : Intramural NIH HHS
ID : ZIA NS003154
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/N026004/1
Pays : United Kingdom
Organisme : Intramural NIH HHS
ID : Z99 AG999999
Pays : United States

Informations de copyright

© 2020 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

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Auteurs

Alexey A Shadrin (AA)

NORMENT, Institute of Clinical Medicine, University of Oslo and Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Sören Mucha (S)

Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany.

David Ellinghaus (D)

Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany.

Mary B Makarious (MB)

Neurodegenerative Diseases Research Unit, National Institute of Neurological Disorders and, Stroke, National Institutes of Health, Bethesda, Maryland, USA.

Cornelis Blauwendraat (C)

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

Ashwin A K Sreelatha (AAK)

Centre for Genetic Epidemiology, Institute for Clinical Epidemiology and Applied Biometry, University of Tübingen, Tübingen, Germany.

Antonio Heras-Garvin (A)

Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria.

Jinhui Ding (J)

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

Monia Hammer (M)

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

Alexandra Foubert-Samier (A)

Service de Neurologie, CRMR Atrophie Multisystématisée, CHU Bordeaux, Bordeaux, France.
Inserm, UMR1219, Bordeaux Population Health Research Center, Bordeaux University, ISPED, Bordeaux, France.

Wassilios G Meissner (WG)

Service de Neurologie, CRMR Atrophie Multisystématisée, CHU Bordeaux, Bordeaux, France.
Univ. de Bordeaux, Institut des Maladies Neurodégénératives, UMR 5293, CNRS, Bordeaux, France.

Olivier Rascol (O)

Centre de Reference Maladie Rare Atrophie MultiSystématisée, Centre d'Investigation, Clinique CIC 1436, Services de Pharmacologie Clinique et Neurosciences, NeuroToul COEN Center, Toulouse, France.
Centre Hospitalo-Universitaire de Toulouse, 3, INSERM, Toulouse, France.

Anne Pavy-Le Traon (A)

Neurology Department, French Reference Centre for MSA, University Hospital of Toulouse and INSERM U 1048, Institute of Cardiovascular and Metabolic Diseases, Toulouse, France.

Oleksandr Frei (O)

NORMENT, Institute of Clinical Medicine, University of Oslo and Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Kevin S O'Connell (KS)

NORMENT, Institute of Clinical Medicine, University of Oslo and Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Shahram Bahrami (S)

NORMENT, Institute of Clinical Medicine, University of Oslo and Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Stefan Schreiber (S)

Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany.
First Medical Department, University Hospital Schleswig-Holstein, Kiel, Germany.

Wolfgang Lieb (W)

Institute of Epidemiology and Biobank PopGen, Christian-Albrechts-University of Kiel, Kiel, Germany.

Martina Müller-Nurasyid (M)

Institute of Genetic Epidemiology, Helmholtz Zentrum München - German Research Center for Environmental Health, Neuherberg, Germany.
Chair of Genetic Epidemiology, IBE, Faculty of Medicine, Ludwig-Maximilians-University (LMU) Munich, Munich, Germany.
Department of Internal Medicine I (Cardiology), Hospital of the Ludwig-Maximilians-University (LMU) Munich, Munich, Germany.

Ulf Schminke (U)

Department of Neurology, University Medicine Greifswald, Greifswald, Germany.

Georg Homuth (G)

Department of Functional Genomics, Interfaculty Institute for Genetics and Functional Genomics, University Medicine and Ernst-Moritz-Arndt-University Greifswald, Greifswald, Germany.

Carsten O Schmidt (CO)

Institute for Community Medicine, Study of Health in Pomerania/KEF, University Medicine Greifswald, Greifswald, Germany.

Markus M Nöthen (MM)

Institute of Human Genetics, University of Bonn, Bonn, Germany.

Per Hoffmann (P)

Institute of Human Genetics, University of Bonn, Bonn, Germany.

Christian Gieger (C)

Research Unit of Molecular Epidemiology, Institute of Epidemiology, Helmholtz Zentrum München-German Research Center for Environmental Health, Neuherberg, Germany.

Gregor Wenning (G)

Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria.

J Raphael Gibbs (JR)

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

Andre Franke (A)

Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany.

John Hardy (J)

Rita Lila Weston Institute, University College London, London, UK.

Nadia Stefanova (N)

Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria.

Thomas Gasser (T)

German Center for Neurodegenerative Diseases (DZNE), Tübingen, Germany.
Department of Neurodegenerative Diseases, Hertie Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany.

Andrew Singleton (A)

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

Henry Houlden (H)

Rita Lila Weston Institute, University College London, London, UK.

Sonja W Scholz (SW)

Neurodegenerative Diseases Research Unit, National Institute of Neurological Disorders and, Stroke, National Institutes of Health, Bethesda, Maryland, USA.
Department of Neurology, Johns Hopkins University Medical Center, Baltimore, Maryland, USA.

Ole A Andreassen (OA)

NORMENT, Institute of Clinical Medicine, University of Oslo and Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.

Manu Sharma (M)

Centre for Genetic Epidemiology, Institute for Clinical Epidemiology and Applied Biometry, University of Tübingen, Tübingen, Germany.

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