The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy

Previous studies have demonstrated neuronal and microglial Fyn, a Src family kinase (SFK), and how its interactions with tau contribute to epileptogenesis. Saracatinib, a Fyn/SFK inhibitor, modifies disease progression in rat kainate (KA) epilepsy models. In this study, we investigated neuronal-spec...

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Main Authors: Nikhil S. Rao, Marson Putra, Christina Meyer, Sirisha Parameswaran, Thimmasettappa Thippeswamy
Format: Article
Language:English
Published: MDPI AG 2025-05-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/14/10/743
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author Nikhil S. Rao
Marson Putra
Christina Meyer
Sirisha Parameswaran
Thimmasettappa Thippeswamy
author_facet Nikhil S. Rao
Marson Putra
Christina Meyer
Sirisha Parameswaran
Thimmasettappa Thippeswamy
author_sort Nikhil S. Rao
collection DOAJ
description Previous studies have demonstrated neuronal and microglial Fyn, a Src family kinase (SFK), and how its interactions with tau contribute to epileptogenesis. Saracatinib, a Fyn/SFK inhibitor, modifies disease progression in rat kainate (KA) epilepsy models. In this study, we investigated neuronal-specific <i>fyn</i> knockdown effects on Fyn–tau signaling, neurodegeneration, and gliosis using a calcium/calmodulin-dependent protein kinase II (CaMKII)-promoter-driven adeno-associated viral vector (AAV9)-mediated <i>fyn</i>-shRNA injection in the rat hippocampus. Eight days following AAV administration, rats received repeated low-dose KA injections intraperitoneally to induce <i>status epilepticus</i> (SE). Both <i>fyn</i>-shRNA and control groups showed comparable SE severity, indicating inadequate neuronal <i>fyn</i> knockdown at this timepoint. Two weeks post <i>fyn</i>-shRNA injection, hippocampal Fyn significantly decreased, alongside reductions in NR2B, pNR2B<sup>Y1472</sup>, PSD95, and total tau. There was also a compensatory activation of SFK (pSFK<sup>Y416</sup>:Fyn) and tau hyperphosphorylation (AT8:total tau), negatively correlating with NeuN expression. Proximity ligation assay indicated unchanged Fyn–tau interactions, suggesting tau interactions with alternative SH3 domain proteins. Persistent neuronal loss, astrogliosis, and microgliosis suggested limited effectiveness of neuronal-specific <i>fyn</i> knockdown at this timepoint. An extended-duration <i>fyn</i> knockdown study, or using broad SFK inhibitors such as saracatinib or tau-SH3 blocking peptides, may effectively prevent SE-induced epileptogenesis.
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spelling doaj-art-b48b5bf8203c40bba520a8efef6f13aa2025-08-20T03:47:53ZengMDPI AGCells2073-44092025-05-01141074310.3390/cells14100743The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe EpilepsyNikhil S. Rao0Marson Putra1Christina Meyer2Sirisha Parameswaran3Thimmasettappa Thippeswamy4Department of Biomedical Sciences, College of Veterinary Medicine, Iowa State University of Science and Technology, Ames, IA 50011, USADepartment of Biomedical Sciences, College of Veterinary Medicine, Iowa State University of Science and Technology, Ames, IA 50011, USADepartment of Biomedical Sciences, College of Veterinary Medicine, Iowa State University of Science and Technology, Ames, IA 50011, USADepartment of Biomedical Sciences, College of Veterinary Medicine, Iowa State University of Science and Technology, Ames, IA 50011, USADepartment of Biomedical Sciences, College of Veterinary Medicine, Iowa State University of Science and Technology, Ames, IA 50011, USAPrevious studies have demonstrated neuronal and microglial Fyn, a Src family kinase (SFK), and how its interactions with tau contribute to epileptogenesis. Saracatinib, a Fyn/SFK inhibitor, modifies disease progression in rat kainate (KA) epilepsy models. In this study, we investigated neuronal-specific <i>fyn</i> knockdown effects on Fyn–tau signaling, neurodegeneration, and gliosis using a calcium/calmodulin-dependent protein kinase II (CaMKII)-promoter-driven adeno-associated viral vector (AAV9)-mediated <i>fyn</i>-shRNA injection in the rat hippocampus. Eight days following AAV administration, rats received repeated low-dose KA injections intraperitoneally to induce <i>status epilepticus</i> (SE). Both <i>fyn</i>-shRNA and control groups showed comparable SE severity, indicating inadequate neuronal <i>fyn</i> knockdown at this timepoint. Two weeks post <i>fyn</i>-shRNA injection, hippocampal Fyn significantly decreased, alongside reductions in NR2B, pNR2B<sup>Y1472</sup>, PSD95, and total tau. There was also a compensatory activation of SFK (pSFK<sup>Y416</sup>:Fyn) and tau hyperphosphorylation (AT8:total tau), negatively correlating with NeuN expression. Proximity ligation assay indicated unchanged Fyn–tau interactions, suggesting tau interactions with alternative SH3 domain proteins. Persistent neuronal loss, astrogliosis, and microgliosis suggested limited effectiveness of neuronal-specific <i>fyn</i> knockdown at this timepoint. An extended-duration <i>fyn</i> knockdown study, or using broad SFK inhibitors such as saracatinib or tau-SH3 blocking peptides, may effectively prevent SE-induced epileptogenesis.https://www.mdpi.com/2073-4409/14/10/743<i>fyn</i> knockdownSrc family kinaseepilepsyneurodegenerationneuroinflammation
spellingShingle Nikhil S. Rao
Marson Putra
Christina Meyer
Sirisha Parameswaran
Thimmasettappa Thippeswamy
The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy
Cells
<i>fyn</i> knockdown
Src family kinase
epilepsy
neurodegeneration
neuroinflammation
title The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy
title_full The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy
title_fullStr The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy
title_full_unstemmed The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy
title_short The Effects of Neuronal <i>Fyn</i> Knockdown in the Hippocampus in the Rat Kainate Model of Temporal Lobe Epilepsy
title_sort effects of neuronal i fyn i knockdown in the hippocampus in the rat kainate model of temporal lobe epilepsy
topic <i>fyn</i> knockdown
Src family kinase
epilepsy
neurodegeneration
neuroinflammation
url https://www.mdpi.com/2073-4409/14/10/743
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