Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids

Abstract In addition to modulating serotonin transport, selective serotonin reuptake inhibitors (SSRIs) have multiple other mechanisms that may contribute to clinical effects, and some of these latter actions prompt repurposing of SSRIs for non-psychiatric indications. In a recent study of the SSRIs...

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Main Authors: Yukitoshi Izumi, Angela M. Reiersen, Eric J. Lenze, Steven J. Mennerick, Charles F. Zorumski
Format: Article
Language:English
Published: Nature Publishing Group 2024-11-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-024-03185-3
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author Yukitoshi Izumi
Angela M. Reiersen
Eric J. Lenze
Steven J. Mennerick
Charles F. Zorumski
author_facet Yukitoshi Izumi
Angela M. Reiersen
Eric J. Lenze
Steven J. Mennerick
Charles F. Zorumski
author_sort Yukitoshi Izumi
collection DOAJ
description Abstract In addition to modulating serotonin transport, selective serotonin reuptake inhibitors (SSRIs) have multiple other mechanisms that may contribute to clinical effects, and some of these latter actions prompt repurposing of SSRIs for non-psychiatric indications. In a recent study of the SSRIs fluvoxamine, fluoxetine and sertraline we found that, unlike the other two SSRIs, sertraline acutely inhibited LTP at a low micromolar concentration through inverse agonism of sigma 1 receptors (S1Rs). In the present studies, we pursued mechanisms contributing to sertraline modulation of LTP in rat hippocampal slices. We found that sertraline partially inhibits synaptic responses mediated by N-methyl-D-aspartate receptors (NMDARs) via effects on NMDARs that contain GluN2B subunits. A selective S1R antagonist (NE-100), but not an S1R agonist (PRE-084) blocked effects on NMDARs, even though both S1R ligands were previously shown to prevent LTP inhibition. Both NE-100 and PRE-084, however, prevented adverse effects of sertraline on one-trial learning. Because of the important role that S1Rs play in modulating endoplasmic reticulum stress, we examined whether inhibitors of cellular stress alter effects of sertraline. We found that two stress inhibitors, ISRIB and quercetin, prevented LTP inhibition, as did inhibitors of the synthesis of endogenous neurosteroids, which are homeostatic regulators of cellular stress. These studies highlight complex effects of sertraline, S1Rs and neurosteroids on hippocampal function and have relevance for understanding therapeutic and adverse drug actions.
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spelling doaj-art-d4224406a23c4044a195a81fbf1748992024-11-24T12:43:55ZengNature Publishing GroupTranslational Psychiatry2158-31882024-11-0114111110.1038/s41398-024-03185-3Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroidsYukitoshi Izumi0Angela M. Reiersen1Eric J. Lenze2Steven J. Mennerick3Charles F. Zorumski4Department of Psychiatry & Taylor Family Institute for Innovative Psychiatric Research, Washington University School of MedicineDepartment of Psychiatry & Taylor Family Institute for Innovative Psychiatric Research, Washington University School of MedicineDepartment of Psychiatry & Taylor Family Institute for Innovative Psychiatric Research, Washington University School of MedicineDepartment of Psychiatry & Taylor Family Institute for Innovative Psychiatric Research, Washington University School of MedicineDepartment of Psychiatry & Taylor Family Institute for Innovative Psychiatric Research, Washington University School of MedicineAbstract In addition to modulating serotonin transport, selective serotonin reuptake inhibitors (SSRIs) have multiple other mechanisms that may contribute to clinical effects, and some of these latter actions prompt repurposing of SSRIs for non-psychiatric indications. In a recent study of the SSRIs fluvoxamine, fluoxetine and sertraline we found that, unlike the other two SSRIs, sertraline acutely inhibited LTP at a low micromolar concentration through inverse agonism of sigma 1 receptors (S1Rs). In the present studies, we pursued mechanisms contributing to sertraline modulation of LTP in rat hippocampal slices. We found that sertraline partially inhibits synaptic responses mediated by N-methyl-D-aspartate receptors (NMDARs) via effects on NMDARs that contain GluN2B subunits. A selective S1R antagonist (NE-100), but not an S1R agonist (PRE-084) blocked effects on NMDARs, even though both S1R ligands were previously shown to prevent LTP inhibition. Both NE-100 and PRE-084, however, prevented adverse effects of sertraline on one-trial learning. Because of the important role that S1Rs play in modulating endoplasmic reticulum stress, we examined whether inhibitors of cellular stress alter effects of sertraline. We found that two stress inhibitors, ISRIB and quercetin, prevented LTP inhibition, as did inhibitors of the synthesis of endogenous neurosteroids, which are homeostatic regulators of cellular stress. These studies highlight complex effects of sertraline, S1Rs and neurosteroids on hippocampal function and have relevance for understanding therapeutic and adverse drug actions.https://doi.org/10.1038/s41398-024-03185-3
spellingShingle Yukitoshi Izumi
Angela M. Reiersen
Eric J. Lenze
Steven J. Mennerick
Charles F. Zorumski
Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
Translational Psychiatry
title Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
title_full Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
title_fullStr Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
title_full_unstemmed Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
title_short Sertraline modulates hippocampal plasticity via sigma 1 receptors, cellular stress and neurosteroids
title_sort sertraline modulates hippocampal plasticity via sigma 1 receptors cellular stress and neurosteroids
url https://doi.org/10.1038/s41398-024-03185-3
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