Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.

Consensus exists that lipids must play key functions in synaptic activity but precise mechanistic information is limited. Acid sphingomyelinase knockout mice (ASMko) are a suitable model to address the role of sphingolipids in synaptic regulation as they recapitulate a mental retardation syndrome, N...

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Main Authors: Paola G Camoletto, Hugo Vara, Laura Morando, Emma Connell, Fabio P Marletto, Maurizio Giustetto, Marco Sassoè-Pognetto, Paul P Van Veldhoven, Maria Dolores Ledesma
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2009-01-01
Series:PLoS ONE
Online Access:https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0005310&type=printable
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author Paola G Camoletto
Hugo Vara
Laura Morando
Emma Connell
Fabio P Marletto
Maurizio Giustetto
Marco Sassoè-Pognetto
Paul P Van Veldhoven
Maria Dolores Ledesma
author_facet Paola G Camoletto
Hugo Vara
Laura Morando
Emma Connell
Fabio P Marletto
Maurizio Giustetto
Marco Sassoè-Pognetto
Paul P Van Veldhoven
Maria Dolores Ledesma
author_sort Paola G Camoletto
collection DOAJ
description Consensus exists that lipids must play key functions in synaptic activity but precise mechanistic information is limited. Acid sphingomyelinase knockout mice (ASMko) are a suitable model to address the role of sphingolipids in synaptic regulation as they recapitulate a mental retardation syndrome, Niemann Pick disease type A (NPA), and their neurons have altered levels of sphingomyelin (SM) and its derivatives. Electrophysiological recordings showed that ASMko hippocampi have increased paired-pulse facilitation and post-tetanic potentiation. Consistently, electron microscopy revealed reduced number of docked vesicles. Biochemical analysis of ASMko synaptic membranes unveiled higher amounts of SM and sphingosine (Se) and enhanced interaction of the docking molecules Munc18 and syntaxin1. In vitro reconstitution assays demonstrated that Se changes syntaxin1 conformation enhancing its interaction with Munc18. Moreover, Se reduces vesicle docking in primary neurons and increases paired-pulse facilitation when added to wt hippocampal slices. These data provide with a novel mechanism for synaptic vesicle control by sphingolipids and could explain cognitive deficits of NPA patients.
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spelling doaj-art-ea6987fcec6c419ea64acb42c9c2419a2025-08-20T02:38:27ZengPublic Library of Science (PLoS)PLoS ONE1932-62032009-01-0144e531010.1371/journal.pone.0005310Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.Paola G CamolettoHugo VaraLaura MorandoEmma ConnellFabio P MarlettoMaurizio GiustettoMarco Sassoè-PognettoPaul P Van VeldhovenMaria Dolores LedesmaConsensus exists that lipids must play key functions in synaptic activity but precise mechanistic information is limited. Acid sphingomyelinase knockout mice (ASMko) are a suitable model to address the role of sphingolipids in synaptic regulation as they recapitulate a mental retardation syndrome, Niemann Pick disease type A (NPA), and their neurons have altered levels of sphingomyelin (SM) and its derivatives. Electrophysiological recordings showed that ASMko hippocampi have increased paired-pulse facilitation and post-tetanic potentiation. Consistently, electron microscopy revealed reduced number of docked vesicles. Biochemical analysis of ASMko synaptic membranes unveiled higher amounts of SM and sphingosine (Se) and enhanced interaction of the docking molecules Munc18 and syntaxin1. In vitro reconstitution assays demonstrated that Se changes syntaxin1 conformation enhancing its interaction with Munc18. Moreover, Se reduces vesicle docking in primary neurons and increases paired-pulse facilitation when added to wt hippocampal slices. These data provide with a novel mechanism for synaptic vesicle control by sphingolipids and could explain cognitive deficits of NPA patients.https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0005310&type=printable
spellingShingle Paola G Camoletto
Hugo Vara
Laura Morando
Emma Connell
Fabio P Marletto
Maurizio Giustetto
Marco Sassoè-Pognetto
Paul P Van Veldhoven
Maria Dolores Ledesma
Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.
PLoS ONE
title Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.
title_full Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.
title_fullStr Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.
title_full_unstemmed Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.
title_short Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18.
title_sort synaptic vesicle docking sphingosine regulates syntaxin1 interaction with munc18
url https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0005310&type=printable
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