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@ARTICLE{Kkali:281103,
author = {Küçükali, Fahri and Hill, Elizabeth and Watzeels, Tijs
and Hummerich, Holger and Campbell, Tracy and Darwent, Lee
and Collins, Steven and Stehmann, Christiane and Kovacs,
Gabor G and Geschwind, Michael D and Frontzek, Karl and
Budka, Herbert and Gelpi, Ellen and Aguzzi, Adriano and van
der Lee, Sven J and van Duijn, Cornelia M and Liberski,
Pawel P and Calero, Miguel and Sanchez-Juan, Pascual and
Bouaziz-Amar, Elodie and Laplanche, Jean-Louis and Haïk,
Stéphane and Brandel, Jean-Phillipe and Mammana, Angela and
Capellari, Sabina and Poleggi, Anna and Ladogana, Anna and
Tiple, Dorina and Zafar, Saima and Booth, Stephanie and
Jansen, Gerard H and Areškevičiūtė, Aušrinė and Lund,
Eva Løbner and Glisic, Katie and Parchi, Piero and Hermann,
Peter and Zerr, Inga and Safar, Jiri and Gambetti, Pierluigi
and Appleby, Brian S and Collinge, John and Sleegers,
Kristel and Mead, Simon},
title = {{M}ultiomic analyses direct hypotheses for
{C}reutzfeldt-{J}akob disease risk genes.},
journal = {Brain},
volume = {148},
number = {9},
issn = {0006-8950},
address = {Oxford},
publisher = {Oxford Univ. Press},
reportid = {DZNE-2025-01064},
pages = {3350 - 3363},
year = {2025},
abstract = {Prions are assemblies of misfolded prion protein that cause
several fatal and transmissible neurodegenerative diseases,
with the most common phenotype in humans being sporadic
Creutzfeldt-Jakob disease (sCJD). Aside from variation of
the prion protein itself, molecular risk factors are not
well understood. Prion and prion-like mechanisms are thought
to underpin common neurodegenerative disorders meaning that
the elucidation of mechanisms could have broad relevance.
Herein we sought to further develop our understanding of the
factors that confer risk of sCJD using a systematic gene
prioritization and functional interpretation pipeline based
on multiomic integrative analyses. We integrated the
published sCJD genome-wide association study summary
statistics with publicly available bulk brain and brain cell
type gene and protein expression datasets. We performed
multiple transcriptome and proteome-wide association studies
and Bayesian genetic colocalization analyses between sCJD
risk association signals and multiple brain molecular
quantitative trait loci signals. We then applied our
systematic gene prioritization pipeline to the obtained
results and nominated prioritized sCJD risk genes with
risk-associated molecular mechanisms in a transcriptome and
proteome-wide manner. Genetic upregulation of both gene and
protein expression of syntaxin-6 (STX6) in the brain was
associated with sCJD risk in multiple datasets, with a
risk-associated gene expression regulation specific to
oligodendrocytes. Similarly, increased gene and protein
expression of protein disulfide isomerase family A member 4
(PDIA4), involved in the unfolded protein response, was
linked to increased disease risk, particularly in excitatory
neurons. Protein expression of mesencephalic astrocyte
derived neurotrophic factor (MANF), involved in protection
against endoplasmic reticulum stress and sulfatide binding
(linking to the enzyme in the final step of sulfatide
synthesis, encoded by sCJD risk gene GAL3ST1), was
identified as protective against sCJD. In total 32 genes
were prioritized into two tiers based on the level of
evidence and confidence for further studies. This study
provides insights into the genetically-associated molecular
mechanisms underlying sCJD susceptibility and prioritizes
several specific hypotheses for exploration beyond the prion
protein itself, as well as beyond the previously highlighted
sCJD risk loci, through the newly prioritized sCJD risk
genes and mechanisms. These findings highlight the
importance of glial cells, sulfatides and the excitatory
neuron unfolded protein response in sCJD pathogenesis.},
keywords = {Creutzfeldt-Jakob Syndrome: genetics / Creutzfeldt-Jakob
Syndrome: metabolism / Humans / Genome-Wide Association
Study / Genetic Predisposition to Disease: genetics /
Transcriptome: genetics / Brain: metabolism / Risk Factors /
multiomics (Other) / neurodegeneration (Other) /
proteome-wide association studies (PWAS) (Other) / sporadic
Creutzfeldt-Jakob disease (sCJD) (Other) /
transcriptome-wide association studies (TWAS) (Other)},
cin = {AG Zerr},
ddc = {610},
cid = {I:(DE-2719)1440011-1},
pnm = {353 - Clinical and Health Care Research (POF4-353)},
pid = {G:(DE-HGF)POF4-353},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:39865733},
pmc = {pmc:PMC12404779},
doi = {10.1093/brain/awaf032},
url = {https://pub.dzne.de/record/281103},
}