Spatial lipidomics reveals demyelination and remyelination dynamics in the mouse brain
Open accessAbstract
Myelin pathology in demyelinating diseases is accompanied by lipid remodeling that remains challenging to characterize at the spatial level using traditional mass spectrometry. We developed an optimized AP-MALDI-Orbitrap MSI pipeline, incorporating sample preparation improvements and mass recalibration, to investigate lipid dynamics in the cuprizone (CPZ) mouse model of demyelination. Dual-modality, untargeted lipid profiling was performed to map spatially resolved lipid alterations during demyelination and spontaneous remyelination in two key brain areas of male mice: corpus callosum (CC) and cortex (Ctx), with lipid identifications benchmarked against 4D-LC-TIMS-MS/MS. Demyelinated regions were identified using Black Gold II staining. Using 1 ppm mass tolerance, we annotated 154 and 133 lipids at the sum-composition level in CC and Ctx, respectively, with 60% validated by LC-MS/MS. Spatial lipid profiling revealed CPZ-induced alterations in sphingolipids, sulfatides, and glycerophospholipids, supported by reanalysis of a published snRNA-seq dataset from a mouse CPZ model. Long-chain ceramides (Cer) and hexosylceramides (HexCer) were reduced in demyelinated regions, with partial, region-specific recovery during remyelination. Short-chain sulfatides (SHexCer), sphingomyelins (SM), and seminolipids transiently increased in the CC during demyelination, while long-chain sulfatides decreased in both CC and Ctx. Additionally, we observed demyelination-induced upregulation of polyunsaturated glycerophospholipids in CC and phosphatidylinositols (PI) in cortex. Lipid subclass changes emerged as reliable markers of both demyelination and remyelination in the mouse brain. Region-specific alterations in lipid metabolism provide new insights into the processes of de- and remyelination. Notably, remyelinated fibers have a distinct lipid profile compared to intact myelin, suggesting that lipid-based therapeutic strategies could improve myelin repair.
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In demyelinating and dysmyelinating models, phosphoinositide distributions within white matter tracts are altered.
“In demyelinating and dysmyelinating models, phosphoinositide distributions within white matter tracts are altered [85–87]”
From PLCγ2 deficiency compromises systemic immune tolerance and erodes myelin homeostasis while enhancing oxidative metabolism in the mouse brain (2026) · cites this paper as [86]
The Results section (page not provided) reports increased phosphatidylinositol (PI) species in the corpus callosum during cuprizone-induced demyelination, supporting altered PI distribution in a white-matter tract. It does not report findings from a dysmyelinating model, and its measurements of PI species do not establish altered distributions of phosphorylated phosphoinositides. (LLM, conf=0.85)
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- Authors
- Opielka, M., Urbanowicz, K., Konieczna-Wolska, K., Müller, E., Krajewski, O., Feucherolles, M., Zhou, Q., Bienkowski, M., Frache, G., Hopf, C., Schirmer, L., Rutkowska, A., & Smolenski, R. T.
- Affiliations
- Gdańsk Medical University (PL)
- Heidelberg University (DE)
- Luxembourg Institute of Science and Technology (LU)
- Technische Hochschule Mannheim (DE)
- Corresponding author
- Rutkowska, Aleksandra
- Smolenski, Ryszard T.
- ORCID
- Venue
- Journal of Lipid Research
- Publisher
- Elsevier BV
- Published
- 2025-11
- Volume
- 66
- Issue
- 11
- Pages
- 100912
- ISSN
- 0022-2275 (ISSN-L)
- PMC
- PMC12684768
- OpenAlex
- W4414484780
- Cited by
- 8
- References
- 94
- Citations by year
- 2026: 6 · 2025: 2
- FWCI
- 5.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Lipid Research (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Narodowe Centrum Nauki (2022/47/D/NZ3/02613)
- Republic of Poland Ministry of Science and Higher Education (SKN/SP/571354/2023)
- Gdański Uniwersytet Medyczny
- Bundesministerium für Forschung, Technologie und Raumfahrt (13FH8I09IA)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Multiple Sclerosis Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Physical Sciences › Chemistry › Spectroscopy › Mass Spectrometry Techniques and Applications
- Keywords
- demyelination, remyelination, myelin lipids, spatial lipidomics, sphingolipids, sulfatide, glycerophospholipids, long-chain ceramides, hexosylceramide, sphingomyelin, seminolipid, phosphatidylinositol, corpus callosum, cerebral cortex, lipid metabolism
- MeSH terms
- Remyelination, Lipidomics, Animals, Brain, Corpus Callosum, Cuprizone, Demyelinating Diseases, Disease Models, Animal, Male, Mice, Inbred C57BL, Myelin Sheath, Lipid Metabolism, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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