Frontiers in Aging Neuroscience (Mar 2022)
Genome-Wide Association Study of Alzheimer’s Disease Brain Imaging Biomarkers and Neuropsychological Phenotypes in the European Medical Information Framework for Alzheimer’s Disease Multimodal Biomarker Discovery Dataset
- Jan Homann,
- Tim Osburg,
- Olena Ohlei,
- Valerija Dobricic,
- Laura Deecke,
- Isabelle Bos,
- Isabelle Bos,
- Rik Vandenberghe,
- Rik Vandenberghe,
- Silvy Gabel,
- Philip Scheltens,
- Charlotte E. Teunissen,
- Sebastiaan Engelborghs,
- Sebastiaan Engelborghs,
- Giovanni Frisoni,
- Giovanni Frisoni,
- Olivier Blin,
- Jill C. Richardson,
- Regis Bordet,
- Alberto Lleó,
- Daniel Alcolea,
- Julius Popp,
- Julius Popp,
- Christopher Clark,
- Gwendoline Peyratout,
- Pablo Martinez-Lage,
- Mikel Tainta,
- Richard J. B. Dobson,
- Richard J. B. Dobson,
- Richard J. B. Dobson,
- Richard J. B. Dobson,
- Richard J. B. Dobson,
- Cristina Legido-Quigley,
- Cristina Legido-Quigley,
- Kristel Sleegers,
- Kristel Sleegers,
- Christine Van Broeckhoven,
- Christine Van Broeckhoven,
- Michael Wittig,
- Andre Franke,
- Christina M. Lill,
- Christina M. Lill,
- Kaj Blennow,
- Kaj Blennow,
- Henrik Zetterberg,
- Henrik Zetterberg,
- Henrik Zetterberg,
- Henrik Zetterberg,
- Simon Lovestone,
- Johannes Streffer,
- Johannes Streffer,
- Mara ten Kate,
- Mara ten Kate,
- Stephanie J. B. Vos,
- Frederik Barkhof,
- Frederik Barkhof,
- Pieter Jelle Visser,
- Pieter Jelle Visser,
- Pieter Jelle Visser,
- Lars Bertram,
- Lars Bertram
Affiliations
- Jan Homann
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Tim Osburg
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Olena Ohlei
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Valerija Dobricic
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Laura Deecke
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Isabelle Bos
- Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Alzheimer Centrum Limburg, Maastricht University, Maastricht, Netherlands
- Isabelle Bos
- Department of Neurology, Alzheimer Center Amsterdam, Amsterdam University Medical Centers, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
- Rik Vandenberghe
- Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium
- Rik Vandenberghe
- Neurology Service, University Hospital Leuven, Leuven, Belgium
- Silvy Gabel
- Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium
- Philip Scheltens
- Department of Neurology, Alzheimer Center Amsterdam, Amsterdam University Medical Centers, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
- Charlotte E. Teunissen
- Neurochemistry Laboratory, Department of Clinical Chemistry, Amsterdam Neuroscience, Amsterdam University Medical Centers, Vrije Universiteit, Amsterdam, Netherlands
- Sebastiaan Engelborghs
- Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium
- Sebastiaan Engelborghs
- Department of Neurology and Center for Neurosciences, Universitair Ziekenhuis Brussel and Vrije Universiteit Brussel (VUB), Brussels, Belgium
- Giovanni Frisoni
- Department of Psychiatry, University of Geneva, Geneva, Switzerland
- Giovanni Frisoni
- 0IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy
- Olivier Blin
- 1Institut Neurosciences Timone, AIX Marseille University, Marseille, France
- Jill C. Richardson
- 2Neurosciences Therapeutic Area, GlaxoSmithKline R&D, Stevenage, United Kingdom
- Regis Bordet
- 3Lille Neuroscience and Cognition, University of Lille, Inserm, CHU Lille, Lille, France
- Alberto Lleó
- 4Memory Unit, Neurology Department, Hospital de Sant Pau, Barcelona and Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
- Daniel Alcolea
- 4Memory Unit, Neurology Department, Hospital de Sant Pau, Barcelona and Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain
- Julius Popp
- 5Department of Geriatric Psychiatry, University Hospital of Psychiatry Zurich, Zurich, Switzerland
- Julius Popp
- 6Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland
- Christopher Clark
- 5Department of Geriatric Psychiatry, University Hospital of Psychiatry Zurich, Zurich, Switzerland
- Gwendoline Peyratout
- 6Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland
- Pablo Martinez-Lage
- 7Department of Neurology, Center for Research and Advanced Therapies, CITA-Alzheimer Foundation, Donostia-San Sebastian, Spain
- Mikel Tainta
- 7Department of Neurology, Center for Research and Advanced Therapies, CITA-Alzheimer Foundation, Donostia-San Sebastian, Spain
- Richard J. B. Dobson
- 8Department of Biostatistics and Health Informatics, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King’s College London, London, United Kingdom
- Richard J. B. Dobson
- 9NIHR Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London, London, United Kingdom
- Richard J. B. Dobson
- 0Health Data Research UK London, University College London, London, United Kingdom
- Richard J. B. Dobson
- 1Institute of Health Informatics, University College London, London, United Kingdom
- Richard J. B. Dobson
- 2NIHR Biomedical Research Centre at University College London Hospitals NHS Foundation Trust, London, United Kingdom
- Cristina Legido-Quigley
- 3Steno Diabetes Center, Copenhagen, Denmark
- Cristina Legido-Quigley
- 4King’s College London, Institute of Pharmaceutical Sciences, London, United Kingdom
- Kristel Sleegers
- 5Complex Genetics of Alzheimer’s Disease Group, Center for Molecular Neurology, VIB, Antwerp, Belgium
- Kristel Sleegers
- 6Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium
- Christine Van Broeckhoven
- 6Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium
- Christine Van Broeckhoven
- 7Neurodegenerative Brain Diseases Group, Center for Molecular Neurology, VIB, Antwerp, Belgium
- Michael Wittig
- 8Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany
- Andre Franke
- 8Institute of Clinical Molecular Biology, Christian-Albrechts-University of Kiel, Kiel, Germany
- Christina M. Lill
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Christina M. Lill
- 9Ageing Epidemiology Research Unit, School of Public Health, Imperial College London, London, United Kingdom
- Kaj Blennow
- 0Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Kaj Blennow
- 1Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden
- Henrik Zetterberg
- 0Department of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Henrik Zetterberg
- 1Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden
- Henrik Zetterberg
- 2Department of Neurodegenerative Disease, University College London, Queen Square Institute of Neurology, Queen Square, London, United Kingdom
- Henrik Zetterberg
- 3UK Dementia Research Institute at University College London, London, United Kingdom
- Simon Lovestone
- 4Department of Psychiatry, University of Oxford, Oxford, United Kingdom
- Johannes Streffer
- 5Reference Center for Biological Markers of Dementia (BIODEM), Institute Born-Bunge, University of Antwerp, Antwerp, Belgium
- Johannes Streffer
- 6Janssen R&D, LLC. Beerse, Belgium
- Mara ten Kate
- Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium
- Mara ten Kate
- 7Department of Radiology and Nuclear Medicine, Amsterdam University Medical Centers, Amsterdam Neuroscience, Amsterdam, Netherlands
- Stephanie J. B. Vos
- Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Alzheimer Centrum Limburg, Maastricht University, Maastricht, Netherlands
- Frederik Barkhof
- 7Department of Radiology and Nuclear Medicine, Amsterdam University Medical Centers, Amsterdam Neuroscience, Amsterdam, Netherlands
- Frederik Barkhof
- 8Institutes of Neurology and Healthcare Engineering, University College London, London, United Kingdom
- Pieter Jelle Visser
- Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Alzheimer Centrum Limburg, Maastricht University, Maastricht, Netherlands
- Pieter Jelle Visser
- Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium
- Pieter Jelle Visser
- 9Division of Neurogeriatrics, Department of Neurobiology, Care Sciences and Society, Karolinska Institutet, Stockholm, Sweden
- Lars Bertram
- Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany
- Lars Bertram
- 0Department of Psychology, University of Oslo, Oslo, Norway
- DOI
- https://doi.org/10.3389/fnagi.2022.840651
- Journal volume & issue
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Vol. 14
Abstract
Alzheimer’s disease (AD) is the most frequent neurodegenerative disease with an increasing prevalence in industrialized, aging populations. AD susceptibility has an established genetic basis which has been the focus of a large number of genome-wide association studies (GWAS) published over the last decade. Most of these GWAS used dichotomized clinical diagnostic status, i.e., case vs. control classification, as outcome phenotypes, without the use of biomarkers. An alternative and potentially more powerful study design is afforded by using quantitative AD-related phenotypes as GWAS outcome traits, an analysis paradigm that we followed in this work. Specifically, we utilized genotype and phenotype data from n = 931 individuals collected under the auspices of the European Medical Information Framework for Alzheimer’s Disease Multimodal Biomarker Discovery (EMIF-AD MBD) study to perform a total of 19 separate GWAS analyses. As outcomes we used five magnetic resonance imaging (MRI) traits and seven cognitive performance traits. For the latter, longitudinal data from at least two timepoints were available in addition to cross-sectional assessments at baseline. Our GWAS analyses revealed several genome-wide significant associations for the neuropsychological performance measures, in particular those assayed longitudinally. Among the most noteworthy signals were associations in or near EHBP1 (EH domain binding protein 1; on chromosome 2p15) and CEP112 (centrosomal protein 112; 17q24.1) with delayed recall as well as SMOC2 (SPARC related modular calcium binding 2; 6p27) with immediate recall in a memory performance test. On the X chromosome, which is often excluded in other GWAS, we identified a genome-wide significant signal near IL1RAPL1 (interleukin 1 receptor accessory protein like 1; Xp21.3). While polygenic score (PGS) analyses showed the expected strong associations with SNPs highlighted in relevant previous GWAS on hippocampal volume and cognitive function, they did not show noteworthy associations with recent AD risk GWAS findings. In summary, our study highlights the power of using quantitative endophenotypes as outcome traits in AD-related GWAS analyses and nominates several new loci not previously implicated in cognitive decline.
Keywords