Blood DNA methylomic signatures associated with CSF biomarkers of Alzheimer's disease in the EMIF-AD study

Rebecca G Smith, Ehsan Pishva, Morteza Kouhsar, Jennifer Imm, Valerija Dobricic, Peter Johannsen, Michael Wittig, Andre Franke, Rik Vandenberghe, Jolien Schaeverbeke, Yvonne Freund-Levi, Lutz Frölich, Philip Scheltens, Charlotte E Teunissen, Giovanni Frisoni, Olivier Blin, Jill C Richardson, Régis Bordet, Sebastiaan Engelborghs, Ellen de RoeckPablo Martinez-Lage, Miren Altuna, Mikel Tainta, Alberto Lleó, Isabel Sala, Julius Popp, Gwendoline Peyratout, Laura Winchester, Alejo Nevado-Holgado, Frans Verhey, Magda Tsolaki, Ulf Andreasson, Kaj Blennow, Henrik Zetterberg, Johannes Streffer, Stephanie J B Vos, Simon Lovestone, Pieter Jelle Visser, Lars Bertram, Katie Lunnon*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

INTRODUCTION: We investigated blood DNA methylation patterns associated with 15 well-established cerebrospinal fluid (CSF) biomarkers of Alzheimer's disease (AD) pathophysiology, neuroinflammation, and neurodegeneration. METHODS: We assessed DNA methylation in 885 blood samples from the European Medical Information Framework for Alzheimer's Disease (EMIF-AD) study using the EPIC array. RESULTS: We identified Bonferroni-significant differential methylation associated with CSF YKL-40 (five loci) and neurofilament light chain (NfL; seven loci) levels, with two of the loci associated with CSF YKL-40 levels correlating with plasma YKL-40 levels. A co-localization analysis showed shared genetic variants underlying YKL-40 DNA methylation and CSF protein levels, with evidence that DNA methylation mediates the association between genotype and protein levels. Weighted gene correlation network analysis identified two modules of co-methylated loci correlated with several amyloid measures and enriched in pathways associated with lipoproteins and development. DISCUSSION: We conducted the most comprehensive epigenome-wide association study (EWAS) of AD-relevant CSF biomarkers to date. Future work should explore the relationship between YKL-40 genotype, DNA methylation, and protein levels in the brain. HIGHLIGHTS: Blood DNA methylation was assessed in the EMIF-AD MBD study. Epigenome-wide association studies (EWASs) were performed for 15 Alzheimer's disease (AD)-relevant cerebrospinal fluid (CSF) biomarker measures. Five Bonferroni-significant loci were associated with YKL-40 levels and seven with neurofilament light chain (NfL). DNA methylation in YKL-40 co-localized with previously reported genetic variation. DNA methylation potentially mediates the effect of single-nucleotide polymorphisms (SNPs) in YKL-40 on CSF protein levels.
Original languageEnglish
Pages (from-to)6722-6739
Number of pages18
JournalAlzheimer's & Dementia
Volume20
Issue number10
Early online date28 Aug 2024
DOIs
Publication statusPublished - Oct 2024

Keywords

  • Alzheimer's disease (AD)
  • DNA methylation
  • YKL-40
  • amyloid
  • biomarker
  • blood
  • cerebrospinal fluid (CSF)
  • epigenetics
  • epigenome-wide association study (EWAS)
  • genome-wide association study (GWAS)
  • methylation quantitative trait loci (mQTL)
  • mild cognitive impairment (MCI)
  • neurofilament light (NfL)
  • protein quantitative trait loci (pQTL)
  • tau

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