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Toward molecular phenotyping of temporal lobe epilepsy by spatial omics.

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Title: Toward molecular phenotyping of temporal lobe epilepsy by spatial omics.
Authors: Vermeulen, Isabeau (AUTHOR), Mohren, Ronny (AUTHOR), Neusinger, Micca (AUTHOR), Dancker, Tobias A. (AUTHOR), Vandenbosch, Michiel (AUTHOR), Beckervordersandforth, Jan (AUTHOR), Balluff, Benjamin (AUTHOR), Van der Hel, Rianna P. (AUTHOR), Schijns, Olaf E. M. G. (AUTHOR), Hoogland, Govert (AUTHOR), Rijkers, Kim (AUTHOR), Cillero‐Pastor, Berta (AUTHOR), de Bruyn, Gwendolyn (AUTHOR), Colon, Albert (AUTHOR), Dings, Jim (AUTHOR), Hendriks, Marc (AUTHOR), Hilkman, Danny (AUTHOR), Hoeberigs, Christianne (AUTHOR), van der Pol, Jochem (AUTHOR), de Jong, Lotte (AUTHOR)
Source: Epilepsia (Series 4). Jul2025, Vol. 66 Issue 7, p2538-2553. 16p.
Subjects: Temporal lobe epilepsy, Mass spectrometry, Lipid analysis, Metabolic profile tests, Proteomics, Multiomics, Individualized medicine
Abstract: Objective: In temporal lobe epilepsy (TLE), detection of the epileptogenic zone predicts a good surgical outcome. When submitted to 18F‐fluorodeoxyglucose positron emission tomography (PET), some patients display lateralized, focal hypometabolism in the temporal lobe (PET+), whereas others appear normometabolic (PET−). However, the mechanism behind this metabolic difference remains unclear. This study aimed to identify differential molecular mechanisms in these patient subtypes. Methods: Neocortical and hippocampal biopsies of TLE patients (n = 3 PET+, n = 3 PET−) and nonepileptic postmortem controls (n = 3) were analyzed for lipid distribution using mass spectrometry imaging (MSI). Laser capture microdissection of the neocortical gray matter and hippocampal cornu ammonis and dentate gyrus was guided by MSI‐derived lipid profiles and histological annotations. Dissected areas were then subjected to liquid chromatography– tandem mass spectrometry‐based label‐free quantitative proteomic analysis. Results: MSI showed distinct lipid profiles, namely, phosphatidylserines were more abundant in PET+ samples in both the neocortex and hippocampus. Proteomic analysis showed significant differences between TLE and nonepileptic postmortem controls involving pathways in neuron excitability and neurotransmitter transporters, which were upregulated in TLE. Compared to PET−, all PET+ specimens displayed significantly dysregulated calcium signaling. Additionally, the neocortex of PET+ patients showed a shift from mitochondrial to cytosolic (cytoplasm of the cell) processes, whereas the hippocampus was characterized by a disruption of glycosylation and polyamine metabolism. Significance: The applied spatial omics approach demonstrated localized molecular differences between metabolic subtypes of TLE patients. These findings may further specify these TLE subtypes and provide leads for targeted treatment. [ABSTRACT FROM AUTHOR]
Copyright of Epilepsia (Series 4) is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract. (Copyright applies to all Abstracts.)
Database: Psychology and Behavioral Sciences Collection
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  Data: Toward molecular phenotyping of temporal lobe epilepsy by spatial omics.
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  Data: <searchLink fieldCode="AR" term="%22Vermeulen%2C+Isabeau%22">Vermeulen, Isabeau</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Mohren%2C+Ronny%22">Mohren, Ronny</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Neusinger%2C+Micca%22">Neusinger, Micca</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Dancker%2C+Tobias+A%2E%22">Dancker, Tobias A.</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Vandenbosch%2C+Michiel%22">Vandenbosch, Michiel</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Beckervordersandforth%2C+Jan%22">Beckervordersandforth, Jan</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Balluff%2C+Benjamin%22">Balluff, Benjamin</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Van+der+Hel%2C+Rianna+P%2E%22">Van der Hel, Rianna P.</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Schijns%2C+Olaf+E%2E+M%2E+G%2E%22">Schijns, Olaf E. M. G.</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Hoogland%2C+Govert%22">Hoogland, Govert</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Rijkers%2C+Kim%22">Rijkers, Kim</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Cillero‐Pastor%2C+Berta%22">Cillero‐Pastor, Berta</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22de+Bruyn%2C+Gwendolyn%22">de Bruyn, Gwendolyn</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Colon%2C+Albert%22">Colon, Albert</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Dings%2C+Jim%22">Dings, Jim</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Hendriks%2C+Marc%22">Hendriks, Marc</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Hilkman%2C+Danny%22">Hilkman, Danny</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22Hoeberigs%2C+Christianne%22">Hoeberigs, Christianne</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22van+der+Pol%2C+Jochem%22">van der Pol, Jochem</searchLink> (AUTHOR)<br /><searchLink fieldCode="AR" term="%22de+Jong%2C+Lotte%22">de Jong, Lotte</searchLink> (AUTHOR)
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  Data: <searchLink fieldCode="JN" term="%22Epilepsia+%28Series+4%29%22">Epilepsia (Series 4)</searchLink>. Jul2025, Vol. 66 Issue 7, p2538-2553. 16p.
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  Data: <searchLink fieldCode="DE" term="%22Temporal+lobe+epilepsy%22">Temporal lobe epilepsy</searchLink><br /><searchLink fieldCode="DE" term="%22Mass+spectrometry%22">Mass spectrometry</searchLink><br /><searchLink fieldCode="DE" term="%22Lipid+analysis%22">Lipid analysis</searchLink><br /><searchLink fieldCode="DE" term="%22Metabolic+profile+tests%22">Metabolic profile tests</searchLink><br /><searchLink fieldCode="DE" term="%22Proteomics%22">Proteomics</searchLink><br /><searchLink fieldCode="DE" term="%22Multiomics%22">Multiomics</searchLink><br /><searchLink fieldCode="DE" term="%22Individualized+medicine%22">Individualized medicine</searchLink>
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: Objective: In temporal lobe epilepsy (TLE), detection of the epileptogenic zone predicts a good surgical outcome. When submitted to 18F‐fluorodeoxyglucose positron emission tomography (PET), some patients display lateralized, focal hypometabolism in the temporal lobe (PET+), whereas others appear normometabolic (PET−). However, the mechanism behind this metabolic difference remains unclear. This study aimed to identify differential molecular mechanisms in these patient subtypes. Methods: Neocortical and hippocampal biopsies of TLE patients (n = 3 PET+, n = 3 PET−) and nonepileptic postmortem controls (n = 3) were analyzed for lipid distribution using mass spectrometry imaging (MSI). Laser capture microdissection of the neocortical gray matter and hippocampal cornu ammonis and dentate gyrus was guided by MSI‐derived lipid profiles and histological annotations. Dissected areas were then subjected to liquid chromatography– tandem mass spectrometry‐based label‐free quantitative proteomic analysis. Results: MSI showed distinct lipid profiles, namely, phosphatidylserines were more abundant in PET+ samples in both the neocortex and hippocampus. Proteomic analysis showed significant differences between TLE and nonepileptic postmortem controls involving pathways in neuron excitability and neurotransmitter transporters, which were upregulated in TLE. Compared to PET−, all PET+ specimens displayed significantly dysregulated calcium signaling. Additionally, the neocortex of PET+ patients showed a shift from mitochondrial to cytosolic (cytoplasm of the cell) processes, whereas the hippocampus was characterized by a disruption of glycosylation and polyamine metabolism. Significance: The applied spatial omics approach demonstrated localized molecular differences between metabolic subtypes of TLE patients. These findings may further specify these TLE subtypes and provide leads for targeted treatment. [ABSTRACT FROM AUTHOR]
– Name: AbstractSuppliedCopyright
  Label:
  Group: Ab
  Data: <i>Copyright of Epilepsia (Series 4) is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites without the copyright holder's express written permission. Additionally, content may not be used with any artificial intelligence tools or machine learning technologies. However, users may print, download, or email articles for individual use. This abstract may be abridged. No warranty is given about the accuracy of the copy. Users should refer to the original published version of the material for the full abstract.</i> (Copyright applies to all Abstracts.)
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        Value: 10.1111/epi.18366
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        Text: English
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