Endosomal sorting protein SNX4 limits synaptic vesicle docking and release

Sorting nexin 4 (SNX4) is an evolutionary conserved organizer of membrane recycling. In neurons, SNX4 accumulates in synapses, but how SNX4 affects synapse function remains unknown. We generated a conditional SNX4 knock-out mouse model and report that SNX4 cKO synapses show enhanced neurotransmissio...

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Main Authors: Josse Poppinga, Nolan J Barrett, L Niels Cornelisse, Matthijs Verhage, Jan RT van Weering
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/97910
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author Josse Poppinga
Nolan J Barrett
L Niels Cornelisse
Matthijs Verhage
Jan RT van Weering
author_facet Josse Poppinga
Nolan J Barrett
L Niels Cornelisse
Matthijs Verhage
Jan RT van Weering
author_sort Josse Poppinga
collection DOAJ
description Sorting nexin 4 (SNX4) is an evolutionary conserved organizer of membrane recycling. In neurons, SNX4 accumulates in synapses, but how SNX4 affects synapse function remains unknown. We generated a conditional SNX4 knock-out mouse model and report that SNX4 cKO synapses show enhanced neurotransmission during train stimulation, while the first evoked EPSC was normal. SNX4 depletion did not affect vesicle recycling, basic autophagic flux, or the levels and localization of SNARE-protein VAMP2/synaptobrevin-2. However, SNX4 depletion affected synapse ultrastructure: an increase in docked synaptic vesicles at the active zone, while the overall vesicle number was normal, and a decreased active zone length. These effects together lead to a substantially increased density of docked vesicles per release site. In conclusion, SNX4 is a negative regulator of synaptic vesicle docking and release. These findings suggest a role for SNX4 in synaptic vesicle recruitment at the active zone.
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spelling doaj-art-19bb95e5cd7e487386f565b01cfab78f2025-08-20T01:58:34ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.97910Endosomal sorting protein SNX4 limits synaptic vesicle docking and releaseJosse Poppinga0https://orcid.org/0009-0002-6809-3832Nolan J Barrett1L Niels Cornelisse2Matthijs Verhage3Jan RT van Weering4https://orcid.org/0000-0001-5259-4945Department of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University, Amsterdam, NetherlandsDepartment of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University, Amsterdam, NetherlandsDepartment of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University, Amsterdam, Netherlands; Department of Human Genetics, CNCR, Amsterdam UMC, Amsterdam, NetherlandsDepartment of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University, Amsterdam, Netherlands; Department of Human Genetics, CNCR, Amsterdam UMC, Amsterdam, NetherlandsDepartment of Functional Genomics, Center for Neurogenomics and Cognitive Research (CNCR), VU University, Amsterdam, Netherlands; Department of Human Genetics, CNCR, Amsterdam UMC, Amsterdam, NetherlandsSorting nexin 4 (SNX4) is an evolutionary conserved organizer of membrane recycling. In neurons, SNX4 accumulates in synapses, but how SNX4 affects synapse function remains unknown. We generated a conditional SNX4 knock-out mouse model and report that SNX4 cKO synapses show enhanced neurotransmission during train stimulation, while the first evoked EPSC was normal. SNX4 depletion did not affect vesicle recycling, basic autophagic flux, or the levels and localization of SNARE-protein VAMP2/synaptobrevin-2. However, SNX4 depletion affected synapse ultrastructure: an increase in docked synaptic vesicles at the active zone, while the overall vesicle number was normal, and a decreased active zone length. These effects together lead to a substantially increased density of docked vesicles per release site. In conclusion, SNX4 is a negative regulator of synaptic vesicle docking and release. These findings suggest a role for SNX4 in synaptic vesicle recruitment at the active zone.https://elifesciences.org/articles/97910neurotranmissionvesicle recruitmentplasticityrecycling endosomehippocampal neuron
spellingShingle Josse Poppinga
Nolan J Barrett
L Niels Cornelisse
Matthijs Verhage
Jan RT van Weering
Endosomal sorting protein SNX4 limits synaptic vesicle docking and release
eLife
neurotranmission
vesicle recruitment
plasticity
recycling endosome
hippocampal neuron
title Endosomal sorting protein SNX4 limits synaptic vesicle docking and release
title_full Endosomal sorting protein SNX4 limits synaptic vesicle docking and release
title_fullStr Endosomal sorting protein SNX4 limits synaptic vesicle docking and release
title_full_unstemmed Endosomal sorting protein SNX4 limits synaptic vesicle docking and release
title_short Endosomal sorting protein SNX4 limits synaptic vesicle docking and release
title_sort endosomal sorting protein snx4 limits synaptic vesicle docking and release
topic neurotranmission
vesicle recruitment
plasticity
recycling endosome
hippocampal neuron
url https://elifesciences.org/articles/97910
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AT nolanjbarrett endosomalsortingproteinsnx4limitssynapticvesicledockingandrelease
AT lnielscornelisse endosomalsortingproteinsnx4limitssynapticvesicledockingandrelease
AT matthijsverhage endosomalsortingproteinsnx4limitssynapticvesicledockingandrelease
AT janrtvanweering endosomalsortingproteinsnx4limitssynapticvesicledockingandrelease