Disentangling the genetic overlap and causal relationships between primary open-angle glaucoma, brain morphology and four major neurodegenerative disorders.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Jun 2023
Historique:
received: 21 12 2022
revised: 21 04 2023
accepted: 28 04 2023
medline: 19 6 2023
pubmed: 19 5 2023
entrez: 18 5 2023
Statut: ppublish

Résumé

Primary open-angle glaucoma (POAG) is an optic neuropathy characterized by progressive degeneration of the optic nerve that leads to irreversible visual impairment. Multiple epidemiological studies suggest an association between POAG and major neurodegenerative disorders (Alzheimer's disease, amyotrophic lateral sclerosis, frontotemporal dementia, and Parkinson's disease). However, the nature of the overlap between neurodegenerative disorders, brain morphology and glaucoma remains inconclusive. In this study, we performed a comprehensive assessment of the genetic and causal relationship between POAG and neurodegenerative disorders, leveraging genome-wide association data from studies of magnetic resonance imaging of the brain, POAG, and four major neurodegenerative disorders. This study found a genetic overlap and causal relationship between POAG and its related phenotypes (i.e., intraocular pressure and optic nerve morphology traits) and brain morphology in 19 regions. We also identified 11 loci with a significant local genetic correlation and a high probability of sharing the same causal variant between neurodegenerative disorders and POAG or its related phenotypes. Of interest, a region on chromosome 17 corresponding to MAPT, a well-known risk locus for Alzheimer's and Parkinson's disease, was shared between POAG, optic nerve degeneration traits, and Alzheimer's and Parkinson's diseases. Despite these local genetic overlaps, we did not identify strong evidence of a causal association between these neurodegenerative disorders and glaucoma. Our findings indicate a distinctive and likely independent neurodegenerative process for POAG involving several brain regions although several POAG or optic nerve degeneration risk loci are shared with neurodegenerative disorders, consistent with a pleiotropic effect rather than a causal relationship between these traits. PG was supported by an NHMRC Investigator Grant (#1173390), SM by an NHMRC Senior Research Fellowship and an NHMRC Program Grant (APP1150144), DM by an NHMRC Fellowship, LP is funded by the NEIEY015473 and EY032559 grants, SS is supported by an NIH-Oxford Cambridge Fellowship and NIH T32 grant (GM136577), APK is supported by a UK Research and Innovation Future Leaders Fellowship, an Alcon Research Institute Young Investigator Award and a Lister Institute for Preventive Medicine Award.

Sections du résumé

BACKGROUND BACKGROUND
Primary open-angle glaucoma (POAG) is an optic neuropathy characterized by progressive degeneration of the optic nerve that leads to irreversible visual impairment. Multiple epidemiological studies suggest an association between POAG and major neurodegenerative disorders (Alzheimer's disease, amyotrophic lateral sclerosis, frontotemporal dementia, and Parkinson's disease). However, the nature of the overlap between neurodegenerative disorders, brain morphology and glaucoma remains inconclusive.
METHOD METHODS
In this study, we performed a comprehensive assessment of the genetic and causal relationship between POAG and neurodegenerative disorders, leveraging genome-wide association data from studies of magnetic resonance imaging of the brain, POAG, and four major neurodegenerative disorders.
FINDINGS RESULTS
This study found a genetic overlap and causal relationship between POAG and its related phenotypes (i.e., intraocular pressure and optic nerve morphology traits) and brain morphology in 19 regions. We also identified 11 loci with a significant local genetic correlation and a high probability of sharing the same causal variant between neurodegenerative disorders and POAG or its related phenotypes. Of interest, a region on chromosome 17 corresponding to MAPT, a well-known risk locus for Alzheimer's and Parkinson's disease, was shared between POAG, optic nerve degeneration traits, and Alzheimer's and Parkinson's diseases. Despite these local genetic overlaps, we did not identify strong evidence of a causal association between these neurodegenerative disorders and glaucoma.
INTERPRETATION CONCLUSIONS
Our findings indicate a distinctive and likely independent neurodegenerative process for POAG involving several brain regions although several POAG or optic nerve degeneration risk loci are shared with neurodegenerative disorders, consistent with a pleiotropic effect rather than a causal relationship between these traits.
FUNDING BACKGROUND
PG was supported by an NHMRC Investigator Grant (#1173390), SM by an NHMRC Senior Research Fellowship and an NHMRC Program Grant (APP1150144), DM by an NHMRC Fellowship, LP is funded by the NEIEY015473 and EY032559 grants, SS is supported by an NIH-Oxford Cambridge Fellowship and NIH T32 grant (GM136577), APK is supported by a UK Research and Innovation Future Leaders Fellowship, an Alcon Research Institute Young Investigator Award and a Lister Institute for Preventive Medicine Award.

Identifiants

pubmed: 37201334
pii: S2352-3964(23)00180-9
doi: 10.1016/j.ebiom.2023.104615
pmc: PMC10206164
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104615

Subventions

Organisme : NIGMS NIH HHS
ID : T32 GM136577
Pays : United States

Informations de copyright

Copyright © 2023 The Author(s). Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests J.W. is a consultant for Allergan, Editas, Maze, Regenxbio and has received sponsored research support from Aerpio Pharmaceuticals Inc. L.R.P. is a consultant for Eyenovia, Twenty, and CharacterBio. A.P.K. is a consultant to Aerie, Allergan, Google Health, Novartis, Reichert, Santen and Thea. S.M. hold stock at Seonix Bio Ltd. S.D.T is supported by the QIMR Statistical Genetics PhD scholarship. All remaining authors declare no competing interests.

Auteurs

Santiago Diaz-Torres (S)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia; Faculty of Medicine, University of Queensland (UQ), Brisbane, QLD, Australia. Electronic address: santiago.diaztorres@qimrberghofer.edu.au.

Weixiong He (W)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.

Jackson Thorp (J)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.

Sahba Seddighi (S)

Nuffield Department of Population Health, Oxford University, Oxford, UK; Medical Scientist Training Program, Johns Hopkins University School of Medicine, Baltimore, MD, USA.

Sean Mullany (S)

Department of Ophthalmology, Flinders University, Flinders Medical Centre, Bedford Park, Australia.

Christopher J Hammond (CJ)

Departments of Ophthalmology & Twin Research and Genetic Epidemiology, King's College London, London, UK.

Pirro G Hysi (PG)

Departments of Ophthalmology & Twin Research and Genetic Epidemiology, King's College London, London, UK.

Louis R Pasquale (LR)

Department of Ophthalmology, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA.

Anthony P Khawaja (AP)

NIHR Biomedical Research Centre, Moorfields Eye Hospital NHS Foundation Trust and UCL Institute of Ophthalmology, London, UK.

Alex W Hewitt (AW)

Menzies Institute for Medical Research, University of Tasmania, Hobart, Tasmania, Australia.

Jamie E Craig (JE)

Department of Ophthalmology, Flinders University, Flinders Medical Centre, Bedford Park, Australia.

David A Mackey (DA)

Centre for Ophthalmology and Visual Science, University of Western Australia, Lions Eye Institute, Australia.

Janey L Wiggs (JL)

Department of Ophthalmology, Harvard Medical School, Boston, 02114, MA, USA.

Cornelia van Duijn (C)

Department of Epidemiology, Erasmus MC Rotterdam, the Netherlands.

Michelle K Lupton (MK)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.

Jue-Sheng Ong (JS)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia.

Stuart MacGregor (S)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia; Faculty of Medicine, University of Queensland (UQ), Brisbane, QLD, Australia.

Puya Gharahkhani (P)

Department of Genetics and Computational Biology, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia; Faculty of Medicine, University of Queensland (UQ), Brisbane, QLD, Australia; School of Biomedical Sciences, Queensland University of Technology (QUT), Brisbane, Australia. Electronic address: Puya.Gharahkhani@qimrberghofer.edu.au.

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Classifications MeSH