TMEM106B and CPOX are genetic determinants of cerebrospinal fluid Alzheimer's disease biomarker levels.


Journal

Alzheimer's & dementia : the journal of the Alzheimer's Association
ISSN: 1552-5279
Titre abrégé: Alzheimers Dement
Pays: United States
ID NLM: 101231978

Informations de publication

Date de publication:
10 2021
Historique:
revised: 16 01 2021
received: 08 07 2020
accepted: 13 02 2021
pubmed: 16 5 2021
medline: 30 12 2021
entrez: 15 5 2021
Statut: ppublish

Résumé

Neurofilament light (NfL), chitinase-3-like protein 1 (YKL-40), and neurogranin (Ng) are biomarkers for Alzheimer's disease (AD) to monitor axonal damage, astroglial activation, and synaptic degeneration, respectively. We performed genome-wide association studies (GWAS) using DNA and cerebrospinal fluid (CSF) samples from the EMIF-AD Multimodal Biomarker Discovery study for discovery, and the Alzheimer's Disease Neuroimaging Initiative study for validation analyses. GWAS were performed for all three CSF biomarkers using linear regression models adjusting for relevant covariates. We identify novel genome-wide significant associations between DNA variants in TMEM106B and CSF levels of NfL, and between CPOX and YKL-40. We confirm previous work suggesting that YKL-40 levels are associated with DNA variants in CHI3L1. Our study provides important new insights into the genetic architecture underlying interindividual variation in three AD-related CSF biomarkers. In particular, our data shed light on the sequence of events regarding the initiation and progression of neuropathological processes relevant in AD.

Identifiants

pubmed: 33991015
doi: 10.1002/alz.12330
doi:

Substances chimiques

Biomarkers 0
CHI3L1 protein, human 0
Chitinase-3-Like Protein 1 0
Membrane Proteins 0
Nerve Tissue Proteins 0
Neurofilament Proteins 0
TMEM106B protein, human 0
neurofilament protein L 0
Neurogranin 132654-77-4

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1628-1640

Subventions

Organisme : Alzheimer's Society
ID : 171
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_PC_17214
Pays : United Kingdom
Organisme : CIHR
Pays : Canada
Organisme : NIA NIH HHS
ID : U01 AG024904
Pays : United States

Informations de copyright

© 2021 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.

Références

Jansen IE, Savage JE, Watanabe K, et al. Genome-wide meta-analysis identifies new loci and functional pathways influencing Alzheimer's disease risk. Nat Genet. 2019;51(3):404-413.
Kunkle BW, Grenier-Boley B, Sims R, et al. Genetic meta-analysis of diagnosed Alzheimer's disease identifies new risk loci and implicates Aβ, tau, immunity and lipid processing. Nat Genet. 2019;51:414-430.
Bertram L, Tanzi RE. Genomic mechanisms in Alzheimer's Disease. Brain Pathol. 2020;30(5):966-977.
Bos I, Vos S, Verhey F, et al. Cerebrospinal fluid biomarkers of neurodegeneration, synaptic integrity, and astroglial activation across the clinical Alzheimer's disease spectrum. Alzheimer's. Dement. 2019;15:644-654.
Yuan A, Nixon RA. Specialized roles of neurofilament proteins in synapses: relevance to neuropsychiatric disorders. Brain Res Bull. 2016;126:334-346.
Yuan A, Rao MV, Veeranna NixonRA. Neurofilaments at a glance. J Cell Sci. 2012;125:3257-3263.
Olsson B, Lautner R, Andreasson U, et al. CSF and blood biomarkers for the diagnosis of Alzheimer's disease: a systematic review and meta-analysis. Lancet Neurol. 2016;15:673-684.
Bridel C, Van Wieringen WN, Zetterberg H, et al. Diagnostic value of cerebrospinal fluid neurofilament light protein in neurology: a systematic review and meta-analysis. JAMA Neurol. 2019;76:1035-1048.
Preische O, Schultz SA, Apel A, et al. Serum neurofilament dynamics predicts neurodegeneration and clinical progression in presymptomatic Alzheimer's disease. Nat Med. 2019;25:277-283.
Molinuevo JL, Ayton S, Batrla R, et al. Current state of Alzheimer's fluid biomarkers. Acta Neuropathol. 2018;136:821-853.
Querol-Vilaseca M, Colom-Cadena M, Pegueroles J, et al. YKL-40 (Chitinase 3-like I) is expressed in a subset of astrocytes in Alzheimer's disease and other tauopathies. J Neuroinflammation. 2017;14:118.
Chang JW, Schumacher E, Coulter PM, Vinters HV, Watson JB. Dendritic translocation of RC3/neurogranin mRNA in normal aging, Alzheimer disease and fronto-temporal dementia. J Neuropathol Exp Neurol. 1997;56:1105-1118.
Scheff SW, Price DA, Schmitt FA, DeKosky ST, Mufson EJ. Synaptic alterations in CA1 in mild Alzheimer's disease and mild cognitive impairment. Neurology. 2007;68:1501-1508.
Slemmon JR, Feng B, Erhardt JA. Small proteins that modulate calmodulin-dependent signal transduction. Mol Neurobiol. 2000;22:099-114.
Tarawneh R, D'Angelo G, Crimmins D, et al. Diagnostic and prognostic utility of the synaptic marker neurogranin in Alzheimer's disease. JAMA Neurol. 2016;73:561-571.
Bos I, Vos S, Vandenberghe R, et al. The EMIF-AD multimodal biomarker discovery study: design, methods and cohort characteristics. Alzheimers Res Ther. 2018;10:64.
Hong S, Prokopenko D, Dobricic V, et al. Genome-wide association study of Alzheimer's disease CSF biomarkers in the EMIF-AD multimodal biomarker discovery dataset. Transl Psychiatry. 2020;10(1):403.
Zetterberg H, Skillbäck T, Mattsson N, et al. Association of cerebrospinal fluid neurofilament light concentration with Alzheimer's disease progression. JAMA Neurol. 2016;73:60-67.
Portelius E, Zetterberg H, Skillbäck T, et al. Cerebrospinal fluid neurogranin: relation to cognition and neurodegeneration in Alzheimer's disease. Brain. 2015;138:3373-3385.
Olsson B, Hertze J, Lautner R, et al. Microglial markers are elevated in the prodromal phase of Alzheimer's disease and vascular dementia. J Alzheimer's Dis. 2013;33:45-53.
Li Y, Willer CJ, Ding J, Scheet P, Abecasis GR. MaCH: using sequence and genotype data to estimate haplotypes and unobserved genotypes. Genet Epidemiol. 2010;34:816-834.
Li Y, Willer C, Sanna S, Abecasis G. Genotype Imputation. Annu Rev Genomics Hum Genet. 2009;10:387-406.
Aulchenko YS, Ripke S, Isaacs A, van Duijn CM. GenABEL: an R library for genome-wide association analysis. Bioinformatics. 2007;23:1294-1296.
Watanabe K, Taskesen E, van Bochoven A, Posthuma D. Functional mapping and annotation of genetic associations with FUMA. Nat Commun. 2017;8:1826.
de Leeuw CA, Mooij JM, Heskes T, Posthuma D. MAGMA: generalized gene-set analysis of GWAS data. PLOS Comput Biol. 2015;11:e1004219.
Purcell S, Neale B, Todd-Brown K, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559-575.
Van Deerlin VM, Sleiman PMA, Martinez-Lage M, et al. Common variants at 7p21 are associated with frontotemporal lobar degeneration with TDP-43 inclusions. Nat Genet. 2010;42:234-239.
Pottier C, Zhou X, Perkerson RB, et al. Potential genetic modifiers of disease risk and age at onset in patients with frontotemporal lobar degeneration and GRN mutations: a genome-wide association study. Lancet Neurol. 2018;17:548-558.
Gaunt TR, Shihab HA, Hemani G, et al. Systematic identification of genetic influences on methylation across the human life course. Genome Biol. 2016;17:61.
Lee JJ, Wedow R, Okbay A, et al. Gene discovery and polygenic prediction from a genome-wide association study of educational attainment in 1.1 million individuals. Nat Genet. 2018;50:1112-1121.
Mez J, Chung J, Jun G, et al. Two novel loci, COBL and SLC10A2, for Alzheimer's disease in African Americans. Alzheimer's. Dement. 2017;13:119-129.
Bulik-Sullivan B, Finucane HK, Anttila V, et al. An atlas of genetic correlations across human diseases and traits. Nat Genet. 2015;47:1236-1241.
Byers SA, Price JP, Cooper JJ, Li Q, Price DH. HEXIM2, a HEXIM1-related protein, regulates positive transcription elongation factor b through association with 7SK. J Biol Chem. 2005;280:16360-16367.
Sasayama D, Hattori K, Ogawa S, et al. Genome-wide quantitative trait loci mapping of the human cerebrospinal fluid proteome. Hum Mol Genet. 2017;26:44-51.
Niu L-D, Xu W, Li J-Q, et al. Genome-wide association study of cerebrospinal fluid neurofilament light levels in non-demented elders. Ann Transl Med. 2019;7:657-657.
Buniello A, Macarthur JAL, Cerezo M, et al. The NHGRI-EBI GWAS Catalog of published genome-wide association studies, targeted arrays and summary statistics 2019. Nucleic Acids Res. 2019;47:D1005-D1012.
Emilsson V, Ilkov M, Lamb JR, et al. Co-regulatory networks of human serum proteins link genetics to disease. Science (80-). 2018;36:769-773.
Mattsson N, Cullen NC, Andreasson U, Zetterberg H, Blennow K. Association between longitudinal plasma neurofilament light and neurodegeneration in patients with Alzheimer's disease. JAMA Neurol. 2019;76:791.
Atamna H, Frey WH. A role for heme in Alzheimer's disease: heme binds amyloid β and has altered metabolism. Proc Natl Acad Sci U S A. 2004;101:11153-11158.
Dwyer BE, Stone M, Zhu X, Perry G, Smith MA. Heme deficiency in Alzheimer's disease: a possible connection to porphyria. J Biomed Biotechnol. 2006;2006:24038.
Sun BB, Maranville JC, Peters JE, et al. Genomic atlas of the human plasma proteome. Nature. 2018;558(7708):73-79.
Suhre K, Arnold M, Bhagwat AM, et al. Connecting genetic risk to disease end points through the human blood plasma proteome. Nat Commun. 2017;8:14357.
Ober C, Tan Z, Sun Y, et al. Effect of variation in CHI3L1 on serum YKL-40 level, risk of asthma, and lung function. N Engl J Med. 2008;358(16):1682-1691.
Willemse EAJ, Vermeiren Y, Garcia-Ayllon MS, et al. Pre-analytical stability of novel cerebrospinal fluid biomarkers. Clin Chim Acta. 2019;497:204-211.

Auteurs

Shengjun Hong (S)

Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany.

Valerija Dobricic (V)

Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany.

Olena Ohlei (O)

Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany.

Isabelle Bos (I)

Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Alzheimer Centrum Limburg, Maastricht University, Maastricht, the Netherlands.
Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, the Netherlands.

Stephanie J B Vos (SJB)

Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Alzheimer Centrum Limburg, Maastricht University, Maastricht, the Netherlands.
Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, the Netherlands.

Dmitry Prokopenko (D)

Genetics and Aging Unit and McCance Center for Brain Health, Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA.

Betty M Tijms (BM)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, the Netherlands.

Ulf Andreasson (U)

Institute of Neuroscience and Physiology, Department of Psychiatry and Neurochemistry, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.

Kaj Blennow (K)

Institute of Neuroscience and Physiology, Department of Psychiatry and Neurochemistry, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.

Rik Vandenberghe (R)

Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium.
Neurology Service, University Hospital Leuven, Leuven, Belgium.

Silvy Gabel (S)

Laboratory for Cognitive Neurology, Department of Neurosciences, KU Leuven, Leuven, Belgium.

Philip Scheltens (P)

Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, the Netherlands.

Charlotte E Teunissen (CE)

Neurochemistry Laboratory, Department of Clinical Chemistry, Amsterdam Neuroscience, Amsterdam University Medical Centers, Vrije Universiteit, Amsterdam, the Netherlands.

Sebastiaan Engelborghs (S)

Department of Biomedical Sciences, Institute Born-Bunge, University of Antwerp, Antwerp, Belgium.
Department of Neurology and Center for Neurosciences, UZ Brussel and Vrije Universiteit Brussel (VUB), Brussels, Belgium.

Giovanni Frisoni (G)

University of Geneva, Geneva, Switzerland.
IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.

Olivier Blin (O)

AIX Marseille University, INS, Ap-hm, Marseille, France.

Jill C Richardson (JC)

Neurosciences Therapeutic Area, GlaxoSmithKline R&D, Stevenage, UK.

Regis Bordet (R)

Inserm, CHU Lille, University of Lille, Lille, France.

Alberto Lleó (A)

Memory Unit, Neurology Department. Hospital de Sant Pau, Barcelona and Centro de Investigación Biomédica en Red en enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain.

Daniel Alcolea (D)

Memory Unit, Neurology Department. Hospital de Sant Pau, Barcelona and Centro de Investigación Biomédica en Red en enfermedades Neurodegenerativas (CIBERNED), Madrid, Spain.

Julius Popp (J)

Centre for Gerontopsychiatric Medicine, Department of Geriatric Psychiatry, University Hospital of Psychiatry Zurich, Zürich, Switzerland.
Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland.

Christopher Clark (C)

Centre for Gerontopsychiatric Medicine, Department of Geriatric Psychiatry, University Hospital of Psychiatry Zurich, Zürich, Switzerland.

Gwendoline Peyratout (G)

Old Age Psychiatry, Department of Psychiatry, University Hospital of Lausanne, Lausanne, Switzerland.

Pablo Martinez-Lage (P)

Department of Neurology, Center for Research and Advanced Therapies, CITA-Alzheimer Foundation, San Sebastian, Spain.

Mikel Tainta (M)

Department of Neurology, Center for Research and Advanced Therapies, CITA-Alzheimer Foundation, San Sebastian, Spain.

Richard J B Dobson (RJB)

Department of Biostatistics and Health Informatics, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
NIHR BioResource Centre Maudsley, NIHR Maudsley Biomedical Research Centre (BRC) at South London and Maudsley NHS Foundation Trust (SLaM) & Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, UK.
Health Data Research UK London, University College London, London, UK.
Institute of Health Informatics, University College London, London, UK.
The National Institute for Health Research University College London Hospitals Biomedical Research Centre, University College London, London, UK.

Cristina Legido-Quigley (C)

Steno Diabetes Center, Copenhagen, Denmark and Institute of Pharmaceutical Sciences, King's College London, London, UK.

Kristel Sleegers (K)

Neurodegenerative Brain Diseases Group, Center for Molecular Neurology, VIB, Antwerp, Belgium.
Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Christine Van Broeckhoven (C)

Neurodegenerative Brain Diseases Group, Center for Molecular Neurology, VIB, Antwerp, Belgium.
Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium.

Rudolph E Tanzi (RE)

Genetics and Aging Unit and McCance Center for Brain Health, Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA.

Mara Ten Kate (M)

Alzheimer Center and Department of Neurology, Amsterdam University Medical Centers, Amsterdam Neuroscience, Amsterdam, the Netherlands.
Department of Radiology and Nuclear Medicine, Amsterdam University Medical Centers, Amsterdam Neuroscience, Amsterdam, the Netherlands.

Michael Wittig (M)

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

Andre Franke (A)

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

Christina M Lill (CM)

Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany.
Ageing Epidemiology Research Unit, School of Public Health, Imperial College, London, United Kingdom.

Frederik Barkhof (F)

Institutes of Neurology and Healthcare Engineering, University College London, London, UK.

Simon Lovestone (S)

Department of Psychiatry, University of Oxford, Oxford, UK.

Johannes Streffer (J)

Reference Center for Biological Markers of Dementia (BIODEM), Institute Born-Bunge, University of Antwerp, Antwerp, Belgium.
Translational Medicine Neuroscience, UCB Biopharma SPRL, Braine l'Alleud, Belgium.

Henrik Zetterberg (H)

Institute of Neuroscience and Physiology, Department of Psychiatry and Neurochemistry, The Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden.
Clinical Neurochemistry Laboratory, Sahlgrenska University Hospital, Mölndal, Sweden.
Department of Neurodegenerative Disease, UCL Queen Square Institute of Neurology, Queen Square, London, UK.
UK Dementia Research Institute at UCL, London, UK.

Pieter Jelle Visser (PJ)

Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience, Alzheimer Centrum Limburg, Maastricht University, Maastricht, the Netherlands.
Alzheimer Center Amsterdam, Department of Neurology, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, Amsterdam UMC, the Netherlands.
Department of Neurobiology, Care Sciences and Society, Division of Neurogeriatrics, Karolinska Instutet, Stockholm, Sweden.

Lars Bertram (L)

Lübeck Interdisciplinary Platform for Genome Analytics (LIGA), University of Lübeck, Lübeck, Germany.
Department of Psychology, University of Oslo, Oslo, Norway.

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