Common Variants Near ZIC1 and ZIC4 in Autopsy-Confirmed Multiple System Atrophy.


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:
10 2022
Historique:
revised: 04 04 2022
received: 24 01 2022
accepted: 02 05 2022
pubmed: 24 8 2022
medline: 19 10 2022
entrez: 23 8 2022
Statut: ppublish

Résumé

Multiple System Atrophy is a rare neurodegenerative disease with alpha-synuclein aggregation in glial cytoplasmic inclusions and either predominant olivopontocerebellar atrophy or striatonigral degeneration, leading to dysautonomia, parkinsonism, and cerebellar ataxia. One prior genome-wide association study in mainly clinically diagnosed patients with Multiple System Atrophy failed to identify genetic variants predisposing for the disease. Since the clinical diagnosis of Multiple System Atrophy yields a high rate of misdiagnosis when compared to the neuropathological gold standard, we studied only autopsy-confirmed cases. We studied common genetic variations in Multiple System Atrophy cases (N = 731) and controls (N = 2898). The most strongly disease-associated markers were rs16859966 on chromosome 3, rs7013955 on chromosome 8, and rs116607983 on chromosome 4 with P-values below 5 × 10 Since mutations of ZIC1 and ZIC4 and paraneoplastic autoantibodies directed against ZIC4 are associated with severe cerebellar dysfunction, we conducted immunohistochemical analyses in brain tissue of the frontal cortex and the cerebellum from 24 Multiple System Atrophy patients. Strong immunohistochemical expression of ZIC4 was detected in a subset of neurons of the dentate nucleus in all healthy controls and in patients with striatonigral degeneration, whereas ZIC4-immunoreactive neurons were significantly reduced inpatients with olivopontocerebellar atrophy. These findings point to a potential ZIC4-mediated vulnerability of neurons in Multiple System Atrophy. © 2022 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 is a rare neurodegenerative disease with alpha-synuclein aggregation in glial cytoplasmic inclusions and either predominant olivopontocerebellar atrophy or striatonigral degeneration, leading to dysautonomia, parkinsonism, and cerebellar ataxia. One prior genome-wide association study in mainly clinically diagnosed patients with Multiple System Atrophy failed to identify genetic variants predisposing for the disease.
OBJECTIVE
Since the clinical diagnosis of Multiple System Atrophy yields a high rate of misdiagnosis when compared to the neuropathological gold standard, we studied only autopsy-confirmed cases.
METHODS
We studied common genetic variations in Multiple System Atrophy cases (N = 731) and controls (N = 2898).
RESULTS
The most strongly disease-associated markers were rs16859966 on chromosome 3, rs7013955 on chromosome 8, and rs116607983 on chromosome 4 with P-values below 5 × 10
INTERPRETATION
Since mutations of ZIC1 and ZIC4 and paraneoplastic autoantibodies directed against ZIC4 are associated with severe cerebellar dysfunction, we conducted immunohistochemical analyses in brain tissue of the frontal cortex and the cerebellum from 24 Multiple System Atrophy patients. Strong immunohistochemical expression of ZIC4 was detected in a subset of neurons of the dentate nucleus in all healthy controls and in patients with striatonigral degeneration, whereas ZIC4-immunoreactive neurons were significantly reduced inpatients with olivopontocerebellar atrophy. These findings point to a potential ZIC4-mediated vulnerability of neurons in Multiple System Atrophy. © 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 35997131
doi: 10.1002/mds.29164
pmc: PMC10052809
mid: NIHMS1869649
doi:

Substances chimiques

Autoantibodies 0
Nerve Tissue Proteins 0
Transcription Factors 0
ZIC1 protein, human 0
ZIC4 protein, human 0
alpha-Synuclein 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2110-2121

Subventions

Organisme : NIA NIH HHS
ID : U24 AG021886
Pays : United States
Organisme : NIA NIH HHS
ID : U01 AG032984
Pays : United States
Organisme : Medical Research Council
ID : MR/L016451/1
Pays : United Kingdom
Organisme : NIA NIH HHS
ID : U01 AG016976
Pays : United States
Organisme : NINDS NIH HHS
ID : P50 NS053488
Pays : United States
Organisme : NIA NIH HHS
ID : P50 AG005136
Pays : United States
Organisme : NIA NIH HHS
ID : U24 AG041689
Pays : United States
Organisme : NIA NIH HHS
ID : P01 AG066597
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG066509
Pays : United States
Organisme : NINDS NIH HHS
ID : U54 NS110435
Pays : United States
Organisme : NINDS NIH HHS
ID : U24 NS120854
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG072979
Pays : United States
Organisme : NIA NIH HHS
ID : K08 AG065463
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG010124
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG072977
Pays : United States
Organisme : NIA NIH HHS
ID : U19 AG062418
Pays : United States

Informations de copyright

© 2022 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

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Auteurs

Franziska Hopfner (F)

Department of Neurology Hannover Medical School, Hannover, Germany.

Anja K Tietz (AK)

Department of Neurology, Kiel University, Kiel, Germany.

Viktoria C Ruf (VC)

Center for Neuropathology and Prion Research, Ludwig-Maximilians-Universität, Munich, Germany.

Owen A Ross (OA)

Department of Neuroscience, Mayo Clinic, Jacksonville, Florida, USA.
Department of Clinical Genomics, Mayo Clinic, Jacksonville, Florida, USA.

Shunsuke Koga (S)

Department of Neuroscience (Neuropathology), Mayo Clinic, Jacksonville, Florida, USA.

Dennis Dickson (D)

Department of Neuroscience (Neuropathology), Mayo Clinic, Jacksonville, Florida, USA.

Adriano Aguzzi (A)

Institute of Neuropathology, University Hospital Zürich, Zürich, Switzerland.

Johannes Attems (J)

Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, United Kingdom.

Thomas Beach (T)

Banner Sun Health Research Institute, Sun City, Arizona, USA.

Allison Beller (A)

Department of Pathology, University of Washington, Seattle, Washington, USA.

William P Cheshire (WP)

Department of Neurology, Mayo Clinic, Jacksonville, Florida, USA.

Vivianna van Deerlin (V)

Department of Pathology and Laboratory Medicine, Penn Neurodegeneration Genomics Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Paula Desplats (P)

Department of Neurosciences, School of Medicine University of California San Diego, La Jolla, California, USA.
Department of Pathology, School of Medicine University of California San Diego, La Jolla, California, USA.

Günther Deuschl (G)

Department of Neurology, Kiel University, Kiel, Germany.

Charles Duyckaerts (C)

Institut du Cerveau, UMR 7225, Sorbonne Université, Paris Brain Institute-ICM, CNRS, AP-HP, Hôpital de la Pitié Salpêtrière, Inserm U1127 DMU Neurosciences, Paris, France.
Brainbank NeuroCEB Neuropathology Network: Plateforme de Ressources Biologiques, Hôpital de La Pitié-Salpêtrière, Bâtiment Roger Baillet, Paris Cedex, France.

David Ellinghaus (D)

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

Valentin Evsyukov (V)

Department of Neurology Hannover Medical School, Hannover, Germany.

Margaret Ellen Flanagan (ME)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Department of Pathology, Northwestern University, Chicago, Illinois, USA.

Andre Franke (A)

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

Matthew P Frosch (MP)

Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA.
Harvard Medical School, Boston, Massachusetts, USA.
Department of Pathology, Massachusetts General Hospital, Boston, Massachusetts, USA.

Marla Gearing (M)

Departments of Pathology and Laboratory Medicine and Neurology, Emory University School of Medicine, Atlanta, Georgia, USA.

Ellen Gelpi (E)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.
Medical University of Vienna, Austrian Reference Center for Human Prion Diseases (OERPE), Vienna, Austria.

Jay A van Gerpen (JA)

Department of Neurology, Mayo Clinic, Jacksonville, Florida, USA.

Bernardino Ghetti (B)

Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana, USA.

Jonathan D Glass (JD)

Department of Neurology, Emory University, Atlanta, Georgia, USA.

Lea T Grinberg (LT)

Memory and Aging Center, Weill Institute for Neurosciences, Department of Neurology, University of California San Francisco, San Francisco, California, USA.
Global Health Institute, University of California, San Francisco, California, USA.
Department of Pathology, University of California, San Francisco, California, USA.
Department of Pathology, University of Sao Paulo Medical School, Sao Paulo, Brazil.

Glenda Halliday (G)

The University of Sydney, School of Medical Sciences, and Brain & Mind Centre, Sydney, New South Wales, Australia.

Ingo Helbig (I)

Department of Biomedical Informatics, Columbia University Irving Medical Center, New York, New York, USA.
Department of Biomedical and Health Informatics, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
Division of Neurology, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
The Epilepsy NeuroGenetics Initiative (ENGIN), Children's Hospital of Philadelphia, Philadelphia, Pennsylvania, USA.
Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Matthias Höllerhage (M)

Department of Neurology Hannover Medical School, Hannover, Germany.

Inge Huitinga (I)

Department of Neuroimmunology, Netherlands Institute for Neuroscience, Amsterdam, the Netherlands.
Brain Plasticity Group, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, the Netherlands.

David John Irwin (DJ)

Department of Neurology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA.

Dirk C Keene (DC)

Department of Pathology, University of Washington, Seattle, Washington, USA.

Gabor G Kovacs (GG)

Division of Neuropathology and Neurochemistry, Department of Neurology, Medical University of Vienna, Vienna, Austria.
Department of Laboratory Medicine and Pathobiology and Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto, Toronto, Ontario, Canada.
Laboratory Medicine Program and Krembil Brain Institute, University Health Network, Toronto, Ontario, Canada.

Edward B Lee (EB)

Department of Pathology and Laboratory Medicine, Translational Neuropathology Research Laboratory Perelman School of Medicine, Philadelphia, Pennsylvania, USA.

Johannes Levin (J)

DZNE - German Center for Neurodegenerative Diseases, Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.
Department of Neurology, Ludwig-Maximilians-Universität München, Munich, Germany.

Maria J Martí (MJ)

Parkinson's Disease and Movement Disorders Unit, Department of Neurology, Hospital Clinic of Barcelona, Barcelona, Spain.
Institut de Neurociències, Maeztu Center, University of Barcelona, Barcelona, Spain.
Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain.
Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Barcelona, Spain.

Ian Mackenzie (I)

Department of Pathology, University of British Columbia, Vancouver, British Columbia, Canada.
Department of Pathology, Vancouver General Hospital, Vancouver, British Columbia, Canada.

Ian McKeith (I)

Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, United Kingdom.

Catriona Mclean (C)

Department of Anatomical Pathology, Alfred Health, Melbourne, Victoria, Australia.

Brit Mollenhauer (B)

Paracelsus-Elena-Klinik, Kassel, Germany.
Department of Neurology, University Medical Center Goettingen, Gottingen, Germany.

Manuela Neumann (M)

Molecular Neuropathology of Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Tübingen, Germany.
Department of Neuropathology, University Hospital of Tübingen, Tübingen, Germany.

Kathy L Newell (KL)

Department of Pathology and Laboratory Medicine, Indiana University School of Medicine, Indianapolis, Indiana, USA.

Alex Pantelyat (A)

Department of Neurology, School of Medicine, Johns Hopkins University, Baltimore, Maryland, USA.

Manuela Pendziwiat (M)

Department of Neuropediatrics, Children's Hospital, University Medical Center Schleswig-Holstein, University of Kiel, Kiel, Germany.
Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany.

Annette Peters (A)

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

Laura Molina Porcel (L)

Neurology Department, Hospital Clinic, IDIBAPS, Barcelona, Spain.

Alberto Rabano (A)

Neuropathology Department, CIEN Foundation, Alzheimer's Centre Queen Sofía Foundation, Madrid, Spain.

Radoslav Matěj (R)

Department of Pathology, 3rd Faculty of Medicine, Charles University, University Hospital Kralovske Vinohrady, Prague, Czech Republic.
Department of Pathology and Molecular Medicine, 3rd Faculty of Medicine, Charles University, Thomayer University Hospital, Prague, Czech Republic.

Alex Rajput (A)

Division of Neurology, Royal University Hospital, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Ali Rajput (A)

Saskatchewan Movement Disorders Program, Saskatchewan Health Authority/University of Saskatchewan, Saskatoon, Saskatchewan, Canada.

Regina Reimann (R)

Institute of Neuropathology, University Hospital Zürich, Zürich, Switzerland.

William K Scott (WK)

John P. Hussman Institute for Human Genomics and Dr. John T. Macdonald Department of Human Genetics, University of Miami, Miller School of Medicine, Miami, Florida, USA.

William Seeley (W)

Memory and Aging Center, Weill Institute for Neurosciences, Department of Neurology, University of California San Francisco, San Francisco, California, USA.
Global Health Institute, University of California, San Francisco, California, USA.
Department of Pathology, University of California, San Francisco, California, USA.

Sashika Selvackadunco (S)

Basic and Clinical Neuroscience Department, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.

Tanya Simuni (T)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Christine Stadelmann (C)

Institute for Neuropathology, University Medical Centre Göttingen, Göttingen, Germany.

Per Svenningsson (P)

Section of Neurology, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden.

Alan Thomas (A)

Translational and Clinical Research Institute, Newcastle University, Newcastle upon Tyne, United Kingdom.

Claudia Trenkwalder (C)

Paracelsus-Elena-Klinik, Kassel, Germany.
Department of Neurosurgery, University Medical Center Goettingen, Goettingen, Germany.

Claire Troakes (C)

Basic and Clinical Neuroscience Department, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, United Kingdom.

John Q Trojanowski (JQ)

Department of Pathology and Laboratory Medicine, Center for Neurodegenerative Disease Research, Perelman School of Medicine, Philadelphia, Pennsylvania, USA.

Ryan J Uitti (RJ)

Department of Neurology, Mayo Clinic, Jacksonville, Florida, USA.

Charles L White (CL)

Pathology, University of Texas Southwestern Medical Center, Dallas, Texas, USA.

Zbigniew K Wszolek (ZK)

Department of Neurology, Mayo Clinic, Jacksonville, Florida, USA.

Tao Xie (T)

Department of Neurology, University of Chicago Medicine, Chicago, Illinois, USA.

Teresa Ximelis (T)

Alzheimer's Disease and Other Cognitive Disorders Unit, Neurology Service, Hospital Clínic, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona, Barcelona, Spain.

Justo Yebenes (J)

Neurological Tissue Bank, Biobanc-Hospital Clínic-IDIBAPS, Barcelona, Spain.
Servicio de Neurología, Hospital Ramón y Cajal de Madrid, Madrid, Spain.

Ulrich Müller (U)

Institute of Human Genetics, JLU-Gießen, Giessen, Germany.

Gerard D Schellenberg (GD)

Department of Pathology and Laboratory Medicine, Penn Neurodegeneration Genomics Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA.

Jochen Herms (J)

Center for Neuropathology and Prion Research, Ludwig-Maximilians-Universität, Munich, Germany.
DZNE - German Center for Neurodegenerative Diseases, Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Gregor Kuhlenbäumer (G)

Department of Neurology, Kiel University, Kiel, Germany.

Günter Höglinger (G)

Department of Neurology Hannover Medical School, Hannover, Germany.
DZNE - German Center for Neurodegenerative Diseases, Munich, Germany.
Zentrum für Systemische Neurowissenschaften, Hannover, Germany.

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