Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses

Summary: The complex cytoarchitecture of neurons poses significant challenges for the maturation of synaptic membrane proteins. It is currently unclear whether locally secreted synaptic proteins bypass the Golgi or whether they traffic through Golgi satellites (GSs). Here, we create a transgenic GS...

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Main Authors: Maria Andres-Alonso, Maximilian Borgmeyer, Hadi Mirzapourdelavar, Jakob Lormann, Kim Klein, Michaela Schweizer, Sabine Hoffmeister-Ullerich, Anja M. Oelschlegel, Alexander Dityatev, Michael R. Kreutz
Format: Article
Language:English
Published: Elsevier 2023-07-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723007039
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author Maria Andres-Alonso
Maximilian Borgmeyer
Hadi Mirzapourdelavar
Jakob Lormann
Kim Klein
Michaela Schweizer
Sabine Hoffmeister-Ullerich
Anja M. Oelschlegel
Alexander Dityatev
Michael R. Kreutz
author_facet Maria Andres-Alonso
Maximilian Borgmeyer
Hadi Mirzapourdelavar
Jakob Lormann
Kim Klein
Michaela Schweizer
Sabine Hoffmeister-Ullerich
Anja M. Oelschlegel
Alexander Dityatev
Michael R. Kreutz
author_sort Maria Andres-Alonso
collection DOAJ
description Summary: The complex cytoarchitecture of neurons poses significant challenges for the maturation of synaptic membrane proteins. It is currently unclear whether locally secreted synaptic proteins bypass the Golgi or whether they traffic through Golgi satellites (GSs). Here, we create a transgenic GS reporter mouse line and show that GSs are widely distributed along dendrites and are capable of mature glycosylation, in particular sialylation. We find that polysialylation of locally secreted NCAM takes place at GSs. Accordingly, in mice lacking a component of trans-Golgi network-to-plasma membrane trafficking, we find fewer GSs and significantly reduced PSA-NCAM levels in distal dendrites of CA1 neurons that receive input from the temporoammonic pathway. Induction of long-term potentiation at those, but not more proximal, synapses is severely impaired. We conclude that GSs serve the need for local mature glycosylation of synaptic membrane proteins in distal dendrites and thereby contribute to rapid changes in synaptic strength.
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spelling doaj.art-cc25592f2ad74310b045450eed535d522023-06-25T04:42:53ZengElsevierCell Reports2211-12472023-07-01427112692Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapsesMaria Andres-Alonso0Maximilian Borgmeyer1Hadi Mirzapourdelavar2Jakob Lormann3Kim Klein4Michaela Schweizer5Sabine Hoffmeister-Ullerich6Anja M. Oelschlegel7Alexander Dityatev8Michael R. Kreutz9Leibniz Group “Dendritic Organelles and Synaptic Function,” Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, Germany; RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany; Corresponding authorLeibniz Group “Dendritic Organelles and Synaptic Function,” Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, Germany; RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, GermanyGerman Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, GermanyLeibniz Group “Dendritic Organelles and Synaptic Function,” Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, Germany; RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, GermanyLeibniz Group “Dendritic Organelles and Synaptic Function,” Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, GermanyCore Facility Morphology und Electron Microscopy, Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, GermanyCore Facility Bioanalytik, Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, GermanyRG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, GermanyGerman Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany; Center for Behavioral Brain Sciences, Otto von Guericke University, 39120 Magdeburg, Germany; Medical Faculty, Otto von Guericke University, 39120 Magdeburg, GermanyLeibniz Group “Dendritic Organelles and Synaptic Function,” Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, 20251 Hamburg, Germany; RG Neuroplasticity, Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany; German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany; Center for Behavioral Brain Sciences, Otto von Guericke University, 39120 Magdeburg, Germany; Corresponding authorSummary: The complex cytoarchitecture of neurons poses significant challenges for the maturation of synaptic membrane proteins. It is currently unclear whether locally secreted synaptic proteins bypass the Golgi or whether they traffic through Golgi satellites (GSs). Here, we create a transgenic GS reporter mouse line and show that GSs are widely distributed along dendrites and are capable of mature glycosylation, in particular sialylation. We find that polysialylation of locally secreted NCAM takes place at GSs. Accordingly, in mice lacking a component of trans-Golgi network-to-plasma membrane trafficking, we find fewer GSs and significantly reduced PSA-NCAM levels in distal dendrites of CA1 neurons that receive input from the temporoammonic pathway. Induction of long-term potentiation at those, but not more proximal, synapses is severely impaired. We conclude that GSs serve the need for local mature glycosylation of synaptic membrane proteins in distal dendrites and thereby contribute to rapid changes in synaptic strength.http://www.sciencedirect.com/science/article/pii/S2211124723007039CP: Cell biologyCP: Neuroscience
spellingShingle Maria Andres-Alonso
Maximilian Borgmeyer
Hadi Mirzapourdelavar
Jakob Lormann
Kim Klein
Michaela Schweizer
Sabine Hoffmeister-Ullerich
Anja M. Oelschlegel
Alexander Dityatev
Michael R. Kreutz
Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses
Cell Reports
CP: Cell biology
CP: Neuroscience
title Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses
title_full Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses
title_fullStr Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses
title_full_unstemmed Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses
title_short Golgi satellites are essential for polysialylation of NCAM and expression of LTP at distal synapses
title_sort golgi satellites are essential for polysialylation of ncam and expression of ltp at distal synapses
topic CP: Cell biology
CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2211124723007039
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