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@ARTICLE{Galvagnion:164070,
author = {Galvagnion, Céline and Marlet, Frederik Ravnkilde and
Cerri, Silvia and Schapira, Anthony H V and Blandini, Fabio
and Di Monte, Donato A},
title = {{S}phingolipid changes in {P}arkinson {L}444{P} {GBA}
mutation fibroblasts promote α-synuclein aggregation.},
journal = {Brain},
volume = {145},
number = {3},
issn = {0006-8950},
address = {Oxford},
publisher = {Oxford Univ. Press},
reportid = {DZNE-2022-00733},
pages = {1038 - 1051},
year = {2022},
note = {(CC BY-NC)},
abstract = {Intraneuronal accumulation of aggregated α-synuclein is a
pathological hallmark of Parkinson's disease. Therefore,
mechanisms capable of promoting α-synuclein deposition bear
important pathogenetic implications. Mutations of the
glucocerebrosidase 1 (GBA) gene represent a prevalent
Parkinson's disease risk factor. They are associated with
loss of activity of a key enzyme involved in lipid
metabolism, glucocerebrosidase, supporting a mechanistic
relationship between abnormal α-synuclein-lipid
interactions and the development of Parkinson pathology. In
this study, the lipid membrane composition of fibroblasts
isolated from control subjects, patients with idiopathic
Parkinson's disease and Parkinson's disease patients
carrying the L444P GBA mutation (PD-GBA) was assayed using
shotgun lipidomics. The lipid profile of PD-GBA fibroblasts
differed significantly from that of control and idiopathic
Parkinson's disease cells. It was characterized by an
overall increase in sphingolipid levels. It also featured a
significant increase in the proportion of ceramide,
sphingomyelin and hexosylceramide molecules with shorter
chain length and a decrease in the percentage of
longer-chain sphingolipids. The extent of this shift was
correlated to the degree of reduction of fibroblast
glucocerebrosidase activity. Lipid extracts from control and
PD-GBA fibroblasts were added to recombinant α-synuclein
solutions. The kinetics of α-synuclein aggregation were
significantly accelerated after addition of PD-GBA extracts
as compared to control samples. Amyloid fibrils collected at
the end of these incubations contained lipids, indicating
α-synuclein-lipid co-assembly. Lipids extracted from
α-synuclein fibrils were also analysed by shotgun
lipidomics. Data revealed that the lipid content of these
fibrils was significantly enriched by shorter-chain
sphingolipids. In a final set of experiments, control and
PD-GBA fibroblasts were incubated in the presence of the
small molecule chaperone ambroxol. This treatment restored
glucocerebrosidase activity and sphingolipid levels and
composition of PD-GBA cells. It also reversed the
pro-aggregation effect that lipid extracts from PD-GBA
fibroblasts had on α-synuclein. Taken together, the
findings of this study indicate that the L444P GBA mutation
and consequent enzymatic loss are associated with a
distinctly altered membrane lipid profile that provides a
biological fingerprint of this mutation in Parkinson
fibroblasts. This altered lipid profile could also be an
indicator of increased risk for α-synuclein aggregate
pathology.},
keywords = {Fibroblasts: metabolism / Glucosylceramidase: genetics /
Glucosylceramidase: metabolism / Humans / Mutation: genetics
/ Parkinson Disease: metabolism / Sphingolipids /
alpha-Synuclein: genetics / alpha-Synuclein: metabolism /
GBA (Other) / Parkinson’s disease (Other) / fibroblasts
(Other) / lipidomics (Other) / α-synuclein (Other) / SNCA
protein, human (NLM Chemicals) / Sphingolipids (NLM
Chemicals) / alpha-Synuclein (NLM Chemicals) / GBA protein,
human (NLM Chemicals) / Glucosylceramidase (NLM Chemicals)},
cin = {AG Di Monte},
ddc = {610},
cid = {I:(DE-2719)1013008},
pnm = {352 - Disease Mechanisms (POF4-352)},
pid = {G:(DE-HGF)POF4-352},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:35362022},
pmc = {pmc:PMC9050548},
doi = {10.1093/brain/awab371},
url = {https://pub.dzne.de/record/164070},
}