Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes

Background: Temporal lobe epilepsy (TLE) is the most common form of drug-resistant epilepsy, often associated with hippocampal sclerosis (HS), which involves selective neuronal loss in the Cornu Ammonis subregion 1 CA1 and CA4 regions of the hippocampus. Granule cells show migration and mossy fiber...

Full description

Saved in:
Bibliographic Details
Main Authors: Melis Onay, Patrick N. Harter, Katherina Weber, Albrecht Piiper, Marcus Czabanka, Karl H. Plate, Thomas M. Freiman, Florian Gessler, Barbara Puhahn-Schmeiser
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Biomedicines
Subjects:
Online Access:https://www.mdpi.com/2227-9059/12/12/2869
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850240479890767872
author Melis Onay
Patrick N. Harter
Katherina Weber
Albrecht Piiper
Marcus Czabanka
Karl H. Plate
Thomas M. Freiman
Florian Gessler
Barbara Puhahn-Schmeiser
author_facet Melis Onay
Patrick N. Harter
Katherina Weber
Albrecht Piiper
Marcus Czabanka
Karl H. Plate
Thomas M. Freiman
Florian Gessler
Barbara Puhahn-Schmeiser
author_sort Melis Onay
collection DOAJ
description Background: Temporal lobe epilepsy (TLE) is the most common form of drug-resistant epilepsy, often associated with hippocampal sclerosis (HS), which involves selective neuronal loss in the Cornu Ammonis subregion 1 CA1 and CA4 regions of the hippocampus. Granule cells show migration and mossy fiber sprouting, though the mechanisms remain unclear. Microglia play a role in neurogenesis and synaptic modulation, suggesting they may contribute to epilepsy. This study examines the role of microglia and axonal guidance molecules in neuronal reorganization in TLE. Methods: Nineteen hippocampal samples from patients with TLE undergoing epilepsy surgery were analyzed. Microglial activity (M1/M2-like microglia) and neuronal guidance molecules were assessed using microscopy and semi-automated techniques. Gene expression was evaluated using the nCounter Expression Profiling method. Results: Neuronal cell loss was correlated with decreased activity of the M1 microglial phenotype. In the CA2 region, neuronal preservation was linked to increased mossy fiber sprouting and microglial presence. Neuronal markers such as Deleted in Colorectal Cancer (DCC) and Synaptopodin were reduced in areas of cell death, while Netrin-1 was elevated in the granule cell layer, potentially influencing mossy fiber sprouting. The nCounter analysis revealed downregulation of genes involved in neuronal activity (e.g., NPAS4, BCL-2, GRIA1) and upregulation of IκB, indicating reduced neuroinflammation. Conclusions: This study suggests reduced neuroinflammation in areas of neuronal loss, while regions with preserved neurons showed mossy fiber sprouting associated with microglia, Netrin-1, and DCC.
format Article
id doaj-art-3e8603961bc746a29f1da5abdbd9bf22
institution OA Journals
issn 2227-9059
language English
publishDate 2024-12-01
publisher MDPI AG
record_format Article
series Biomedicines
spelling doaj-art-3e8603961bc746a29f1da5abdbd9bf222025-08-20T02:00:51ZengMDPI AGBiomedicines2227-90592024-12-011212286910.3390/biomedicines12122869Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression ChangesMelis Onay0Patrick N. Harter1Katherina Weber2Albrecht Piiper3Marcus Czabanka4Karl H. Plate5Thomas M. Freiman6Florian Gessler7Barbara Puhahn-Schmeiser8Department of Internal Medicine I, Goethe University, Theodor-Stern-Kai 7, 60596 Frankfurt am Main, GermanyDepartment of Neuropathology, Ludwig-Maximillians-University Munich, Feodor-Lynen-Str. 23, 81377 Munich, GermanyDepartment of Neuropathology (Edinger Institute), Goethe University, Heinrich-Hoffmann-Straße 7, 60528 Frankfurt am Main, GermanyDepartment of Internal Medicine I, Goethe University, Theodor-Stern-Kai 7, 60596 Frankfurt am Main, GermanyDepartment of Neurosurgery, Goethe University, Schleusenweg 16, 60528 Frankfurt am Main, GermanyDepartment of Neuropathology (Edinger Institute), Goethe University, Heinrich-Hoffmann-Straße 7, 60528 Frankfurt am Main, GermanyDepartment of Neurosurgery, Rostock University Medical Center, Schilingallee 35, 18057 Rostock, GermanyDepartment of Neurosurgery, Rostock University Medical Center, Schilingallee 35, 18057 Rostock, GermanyDepartment of Neurosurgery, Freiburg University Medical Center, Breisacher Str. 64, 79106 Freiburg, GermanyBackground: Temporal lobe epilepsy (TLE) is the most common form of drug-resistant epilepsy, often associated with hippocampal sclerosis (HS), which involves selective neuronal loss in the Cornu Ammonis subregion 1 CA1 and CA4 regions of the hippocampus. Granule cells show migration and mossy fiber sprouting, though the mechanisms remain unclear. Microglia play a role in neurogenesis and synaptic modulation, suggesting they may contribute to epilepsy. This study examines the role of microglia and axonal guidance molecules in neuronal reorganization in TLE. Methods: Nineteen hippocampal samples from patients with TLE undergoing epilepsy surgery were analyzed. Microglial activity (M1/M2-like microglia) and neuronal guidance molecules were assessed using microscopy and semi-automated techniques. Gene expression was evaluated using the nCounter Expression Profiling method. Results: Neuronal cell loss was correlated with decreased activity of the M1 microglial phenotype. In the CA2 region, neuronal preservation was linked to increased mossy fiber sprouting and microglial presence. Neuronal markers such as Deleted in Colorectal Cancer (DCC) and Synaptopodin were reduced in areas of cell death, while Netrin-1 was elevated in the granule cell layer, potentially influencing mossy fiber sprouting. The nCounter analysis revealed downregulation of genes involved in neuronal activity (e.g., NPAS4, BCL-2, GRIA1) and upregulation of IκB, indicating reduced neuroinflammation. Conclusions: This study suggests reduced neuroinflammation in areas of neuronal loss, while regions with preserved neurons showed mossy fiber sprouting associated with microglia, Netrin-1, and DCC.https://www.mdpi.com/2227-9059/12/12/2869temporal lobe epilepsyhippocampal sclerosismicrogliaM1 phenotypeM2 phenotypeNetrin-1
spellingShingle Melis Onay
Patrick N. Harter
Katherina Weber
Albrecht Piiper
Marcus Czabanka
Karl H. Plate
Thomas M. Freiman
Florian Gessler
Barbara Puhahn-Schmeiser
Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes
Biomedicines
temporal lobe epilepsy
hippocampal sclerosis
microglia
M1 phenotype
M2 phenotype
Netrin-1
title Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes
title_full Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes
title_fullStr Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes
title_full_unstemmed Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes
title_short Mossy Fiber Sprouting in Temporal Lobe Epilepsy: The Impact of Netrin-1, DCC, and Gene Expression Changes
title_sort mossy fiber sprouting in temporal lobe epilepsy the impact of netrin 1 dcc and gene expression changes
topic temporal lobe epilepsy
hippocampal sclerosis
microglia
M1 phenotype
M2 phenotype
Netrin-1
url https://www.mdpi.com/2227-9059/12/12/2869
work_keys_str_mv AT melisonay mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT patricknharter mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT katherinaweber mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT albrechtpiiper mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT marcusczabanka mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT karlhplate mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT thomasmfreiman mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT floriangessler mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges
AT barbarapuhahnschmeiser mossyfibersproutingintemporallobeepilepsytheimpactofnetrin1dccandgeneexpressionchanges