A novel Alzheimer disease locus located near the gene encoding tau protein View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2015-03-17

AUTHORS

G Jun, C A Ibrahim-Verbaas, M Vronskaya, J-C Lambert, J Chung, A C Naj, B W Kunkle, L-S Wang, J C Bis, C Bellenguez, D Harold, K L Lunetta, A L Destefano, B Grenier-Boley, R Sims, G W Beecham, A V Smith, V Chouraki, K L Hamilton-Nelson, M A Ikram, N Fievet, N Denning, E R Martin, H Schmidt, Y Kamatani, M L Dunstan, O Valladares, A R Laza, D Zelenika, A Ramirez, T M Foroud, S-H Choi, A Boland, T Becker, W A Kukull, S J van der Lee, F Pasquier, C Cruchaga, D Beekly, A L Fitzpatrick, O Hanon, M Gill, R Barber, V Gudnason, D Campion, S Love, D A Bennett, N Amin, C Berr, Magda Tsolaki, J D Buxbaum, O L Lopez, V Deramecourt, N C Fox, L B Cantwell, L Tárraga, C Dufouil, J Hardy, P K Crane, G Eiriksdottir, D Hannequin, R Clarke, D Evans, T H Mosley, L Letenneur, C Brayne, W Maier, P De Jager, V Emilsson, J-F Dartigues, H Hampel, M I Kamboh, R F A G de Bruijn, C Tzourio, P Pastor, E B Larson, J I Rotter, M C O'Donovan, T J Montine, M A Nalls, S Mead, E M Reiman, P V Jonsson, C Holmes, P H St George-Hyslop, M Boada, P Passmore, J R Wendland, R Schmidt, K Morgan, A R Winslow, J F Powell, M Carasquillo, S G Younkin, J Jakobsdóttir, J S K Kauwe, K C Wilhelmsen, D Rujescu, M M Nöthen, A Hofman, L Jones, J L Haines, B M Psaty, C Van Broeckhoven, P Holmans, L J Launer, R Mayeux, M Lathrop, A M Goate, V Escott-Price, S Seshadri, M A Pericak-Vance, P Amouyel, J Williams, C M van Duijn, G D Schellenberg, L A Farrer

ABSTRACT

APOE ɛ4, the most significant genetic risk factor for Alzheimer disease (AD), may mask effects of other loci. We re-analyzed genome-wide association study (GWAS) data from the International Genomics of Alzheimer’s Project (IGAP) Consortium in APOE ɛ4+ (10 352 cases and 9207 controls) and APOE ɛ4− (7184 cases and 26 968 controls) subgroups as well as in the total sample testing for interaction between a single-nucleotide polymorphism (SNP) and APOE ɛ4 status. Suggestive associations (P<1 × 10-4) in stage 1 were evaluated in an independent sample (stage 2) containing 4203 subjects (APOE ɛ4+: 1250 cases and 536 controls; APOE ɛ4−: 718 cases and 1699 controls). Among APOE ɛ4− subjects, novel genome-wide significant (GWS) association was observed with 17 SNPs (all between KANSL1 and LRRC37A on chromosome 17 near MAPT) in a meta-analysis of the stage 1 and stage 2 data sets (best SNP, rs2732703, P=5·8 × 10−9). Conditional analysis revealed that rs2732703 accounted for association signals in the entire 100-kilobase region that includes MAPT. Except for previously identified AD loci showing stronger association in APOE ɛ4+ subjects (CR1 and CLU) or APOE ɛ4− subjects (MS4A6A/MS4A4A/MS4A6E), no other SNPs were significantly associated with AD in a specific APOE genotype subgroup. In addition, the finding in the stage 1 sample that AD risk is significantly influenced by the interaction of APOE with rs1595014 in TMEM106B (P=1·6 × 10−7) is noteworthy, because TMEM106B variants have previously been associated with risk of frontotemporal dementia. Expression quantitative trait locus analysis revealed that rs113986870, one of the GWS SNPs near rs2732703, is significantly associated with four KANSL1 probes that target transcription of the first translated exon and an untranslated exon in hippocampus (P⩽1.3 × 10-8), frontal cortex (P⩽1.3 × 10-9) and temporal cortex (P⩽1.2 × 10−11). Rs113986870 is also strongly associated with a MAPT probe that targets transcription of alternatively spliced exon 3 in frontal cortex (P=9.2 × 10−6) and temporal cortex (P=2.6 × 10−6). Our APOE-stratified GWAS is the first to show GWS association for AD with SNPs in the chromosome 17q21.31 region. Replication of this finding in independent samples is needed to verify that SNPs in this region have significantly stronger effects on AD risk in persons lacking APOE ɛ4 compared with persons carrying this allele, and if this is found to hold, further examination of this region and studies aimed at deciphering the mechanism(s) are warranted. More... »

PAGES

108-117

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  • Journal

    TITLE

    Molecular Psychiatry

    ISSUE

    1

    VOLUME

    21

    Author Affiliations

  • Department of Biostatistics, Boston University School of Public Health, Boston, MA, USA
  • Department of Neurology, Erasmus University Medical Center, Erasmus, Rotterdam, The Netherlands
  • Institute of Psychological Medicine and Clinical Neurosciences, Medical Research Council (MRC) Centre for Neuropsychiatric Genetics and Genomics, Cardiff University, Cardiff, UK
  • Institut Pasteur de Lille, Lille, France
  • Department of Medicine (Biomedical Genetics), Boston University School of Medicine, Boston, MA, USA
  • Department of Pathology and Laboratory Medicine, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA
  • The John P. Hussman Institute for Human Genomics, University of Miami, Miami, FL, USA
  • Department of Medicine, Cardiovascular Health Research Unit, University of Washington, Seattle, WA, USA
  • Trinity College, University of Dublin, Dublin, Ireland
  • Macdonald Foundation Department of Human Genetics, University of Miami, Miami, FL, USA
  • Icelandic Heart Association, Kopavogur, Iceland
  • Department of Neurology, Boston University School of Medicine, Boston, MA, USA
  • Department of Radiology, Erasmus University Medical Center, Erasmus, Rotterdam, The Netherlands
  • Institute for Molecular Biology and Biochemistry, Medical University of Graz, Graz, Austria
  • Foundation Jean Dausset—CEPH, Paris, France
  • Memory Clinic of Fundació ACE, Institut Català de Neurociències Aplicades, Barcelona, Spain
  • Centre National de Genotypage, Institut Genomique, Commissariat a l’energie Atomique, Evry, France
  • Institute of Human Genetics, University of Bonn, Bonn, Germany
  • Department of Medical and Molecular Genetics, Indiana University, Indianapolis, IN, USA
  • Institute for Medical Biometry, Informatics and Epidemiology, University of Bonn, Bonn, Germany
  • Department of Epidemiology, University of Washington, Seattle, WA, USA
  • Department of Epidemiology, Erasmus University Medical Center, Erasmus, Rotterdam, The Netherlands
  • Centre National de Reference pour les Malades Alzheimer Jeunes (CNR-MAJ), Centre Hospitalier Régional Universitaire de Lille, Lille, France
  • Department of Psychiatry, Washington University School of Medicine, St Louis, MO, USA
  • National Alzheimer’s Coordinating Center, University of Washington, Seattle, WA, USA
  • Departments of Health Services, University of Washington, Seattle, WA, USA
  • Geriatrics Department, Broca Hospital, Paris, France
  • Mercer’s Institute for Research on Aging, St James Hospital and Trinity College, Dublin, Ireland
  • Department of Pharmacology and Neuroscience, University of North Texas Health Science Center, Fort Worth, TX, USA
  • University of Bristol Institute of Clinical Neurosciences, School of Clinical Sciences, Frenchay Hospital, Bristol, UK
  • Rush Alzheimer’s Disease Center, Rush University Medical Center, Chicago, IL, USA
  • Inserm U888, Hôpital La Colombière, Montpellier, France
  • Department of Neurology, Aristotle University of Thessaloniki, Thessaloniki, Greece
  • Departments of Genetics and Genomic Sciences, Mount Sinai School of Medicine, New York, NY, USA
  • Departments of Neurology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
  • Department of Neurodegenerative Disease, Dementia Research Centre, University College London Institute of Neurology, London, UK
  • Inserm U897, Victor Segalen University, F-33076, Bordeaux, France
  • Reta Lilla Weston Laboratories, Institute of Neurology, London, UK
  • Department of Medicine, University of Washington, Seattle, WA, USA
  • Oxford Healthy Aging Project (OHAP), Clinical Trial Service Unit, University of Oxford, Oxford, UK
  • Department of Internal Medicine, Rush Institute for Healthy Aging, Rush University Medical Center, Chicago, IL, USA
  • Department of Medicine (Geriatrics), University of Mississippi Medical Center, Jackson, MS, USA
  • Institute of Public Health, University of Cambridge, Cambridge, UK
  • German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany
  • Program in Medical and Population Genetics, Broad Institute, Cambridge, MA, USA
  • Faculty of Pharmaceutical Sciences, University of Iceland, Reykjavik, Iceland
  • Centre de Mémoire de Ressources et de Recherche de Bordeaux, CHU de Bordeaux, Bordeaux, France
  • Department of Psychiatry, Ludwig Maximilians University, Munich, Germany
  • Department of Human Genetics, University of Pittsburgh, Pittsburgh, PA, USA
  • CIBERNED, Instituto de Salud Carlos III, Madrid, Spain
  • Group Health, Group Health Research Institute, Seattle, WA, USA
  • Division of Genetic Outcomes, Department of Pediatrics, Harbor-UCLA Medical Center, Torrance, CA, USA
  • Department of Pathology, University of Washington, Seattle, WA, USA
  • Laboratory of Neurogenetics, Intramural Research Program, National Institute on Aging, Bethesda, MD, USA
  • Department of Molecular Neuroscience, Institute of Neurology, London, UK
  • Neurogenomics Division, Translational Genomics Research Institute, Phoenix, Arizona
  • Department of Geriatrics, Landspitali National University Hospital, Reykjavik, Iceland
  • Division of Clinical Neurosciences, School of Medicine, University of Southampton, Southampton, UK
  • Cambridge Institute for Medical Research and Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK
  • Ageing Group, Centre for Public Health, School of Medicine, Dentistry and Biomedical Sciences, Queen’s University, Belfast, UK
  • PharmaTherapeutics Clinical Research, Pfizer Worldwide Research and Development, Cambridge, MA, USA
  • Department of Neurology, Medical University of Graz, Graz, Austria
  • Institute of Genetics, Queen’s Medical Centre, University of Nottingham, Nottingham, UK
  • Department of Neuroscience, King’s College London, Institute of Psychiatry, De Crespigny Park, Denmark Hill, London, UK
  • Department of Neuroscience, Mayo Clinic, Jacksonville, FL, USA
  • Department of Biology, Brigham Young University, Provo, Utah, USA
  • Department of Genetics, University of North Carolina Chapel Hill, Chapel Hill, NC, USA
  • Department of Psychiatry, Psychotherapy and Psychosomatics Martin-Luther-University Halle-Wittenberg, Halle, Germany
  • Department of Genomics, Institute of Human Genetics, Life and Brain Center, University of Bonn, Bonn, Germany
  • Department of Epidemiology and Biostatistics, Case Western Reserve University, Cleveland, OH, USA
  • Institute Born-Bunge, University of Antwerp, Antwerp, Belgium
  • Laboratory of Epidemiology, Demography, and Biometry, National Institute of Health, Bethesda, MD, USA
  • Department of Neurology, Columbia University, New York, NY, USA
  • McGill University and Génome Québec Innovation Centre, Montreal, QC, Canada
  • University Hospital, CHRU Lille, Lille, France
  • Department of Epidemiology, Boston University School of Public Health, Boston, MA, USA
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1038/mp.2015.23

    DOI

    http://dx.doi.org/10.1038/mp.2015.23

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1037355133

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/25778476


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        "description": "APOE \u025b4, the most significant genetic risk factor for Alzheimer disease (AD), may mask effects of other loci. We re-analyzed genome-wide association study (GWAS) data from the International Genomics of Alzheimer\u2019s Project (IGAP) Consortium in APOE \u025b4+ (10\u2009352 cases and 9207 controls) and APOE \u025b4\u2212 (7184 cases and 26\u2009968 controls) subgroups as well as in the total sample testing for interaction between a single-nucleotide polymorphism (SNP) and APOE \u025b4 status. Suggestive associations (P<1 \u00d7 10-4) in stage 1 were evaluated in an independent sample (stage 2) containing 4203 subjects (APOE \u025b4+: 1250 cases and 536 controls; APOE \u025b4\u2212: 718 cases and 1699 controls). Among APOE \u025b4\u2212 subjects, novel genome-wide significant (GWS) association was observed with 17 SNPs (all between KANSL1 and LRRC37A on chromosome 17 near MAPT) in a meta-analysis of the stage 1 and stage 2 data sets (best SNP, rs2732703, P=5\u00b78 \u00d7 10\u22129). Conditional analysis revealed that rs2732703 accounted for association signals in the entire 100-kilobase region that includes MAPT. Except for previously identified AD loci showing stronger association in APOE \u025b4+ subjects (CR1 and CLU) or APOE \u025b4\u2212 subjects (MS4A6A/MS4A4A/MS4A6E), no other SNPs were significantly associated with AD in a specific APOE genotype subgroup. In addition, the finding in the stage 1 sample that AD risk is significantly influenced by the interaction of APOE with rs1595014 in TMEM106B (P=1\u00b76 \u00d7 10\u22127) is noteworthy, because TMEM106B variants have previously been associated with risk of frontotemporal dementia. Expression quantitative trait locus analysis revealed that rs113986870, one of the GWS SNPs near rs2732703, is significantly associated with four KANSL1 probes that target transcription of the first translated exon and an untranslated exon in hippocampus (P\u2a7d1.3 \u00d7 10-8), frontal cortex (P\u2a7d1.3 \u00d7 10-9) and temporal cortex (P\u2a7d1.2 \u00d7 10\u221211). Rs113986870 is also strongly associated with a MAPT probe that targets transcription of alternatively spliced exon 3 in frontal cortex (P=9.2 \u00d7 10\u22126) and temporal cortex (P=2.6 \u00d7 10\u22126). Our APOE-stratified GWAS is the first to show GWS association for AD with SNPs in the chromosome 17q21.31 region. Replication of this finding in independent samples is needed to verify that SNPs in this region have significantly stronger effects on AD risk in persons lacking APOE \u025b4 compared with persons carrying this allele, and if this is found to hold, further examination of this region and studies aimed at deciphering the mechanism(s) are warranted.", 
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        "keywords": [
          "single nucleotide polymorphisms", 
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          "expression quantitative trait loci (eQTL) analysis", 
          "quantitative trait locus (QTL) analysis", 
          "genome-wide significant association", 
          "genome-wide association study data", 
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          "hippocampus", 
          "interaction of apoE", 
          "frontal cortex", 
          "risk", 
          "sample testing", 
          "study data", 
          "examination", 
          "testing", 
          "dementia", 
          "temporal cortex", 
          "subjects", 
          "risk factors", 
          "persons"
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        "name": "A novel Alzheimer disease locus located near the gene encoding tau protein", 
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