Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome

Activity-driven changes in the neuronal surface glycoproteome are known to occur with synapse formation, plasticity, and related diseases, but their mechanistic basis and significance are unclear. Here, we observed that N-glycans on surface glycoproteins of dendrites shift from immature to mature fo...

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Autores principales:	Anitha P Govind, Okunola Jeyifous, Theron A Russell, Zola Yi, Aubrey V Weigel, Abhijit Ramaprasad, Luke Newell, William Ramos, Fernando M Valbuena, Jason C Casler, Jing-Zhi Yan, Benjamin S Glick, Geoffrey T Swanson, Jennifer Lippincott-Schwartz, William N Green
Formato:	article
Lenguaje:	EN
Publicado:	eLife Sciences Publications Ltd 2021
Materias:	Golgi sialic acid glycosylation nicotine neuronal activity Golgi satellites Medicine R Science Q Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/00279d88468b4f06978613bb9f77744b
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spelling	oai:doaj.org-article:00279d88468b4f06978613bb9f77744b2021-11-26T07:05:43ZActivity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome10.7554/eLife.689102050-084Xe68910https://doaj.org/article/00279d88468b4f06978613bb9f77744b2021-09-01T00:00:00Zhttps://elifesciences.org/articles/68910https://doaj.org/toc/2050-084XActivity-driven changes in the neuronal surface glycoproteome are known to occur with synapse formation, plasticity, and related diseases, but their mechanistic basis and significance are unclear. Here, we observed that N-glycans on surface glycoproteins of dendrites shift from immature to mature forms containing sialic acid in response to increased neuronal activation. In exploring the basis of these N-glycosylation alterations, we discovered that they result from the growth and proliferation of Golgi satellites scattered throughout the dendrite. Golgi satellites that formed during neuronal excitation were in close association with endoplasmic reticulum (ER) exit sites and early endosomes and contained glycosylation machinery without the Golgi structural protein, GM130. They functioned as distal glycosylation stations in dendrites, terminally modifying sugars either on newly synthesized glycoproteins passing through the secretory pathway or on surface glycoproteins taken up from the endocytic pathway. These activities led to major changes in the dendritic surface of excited neurons, impacting binding and uptake of lectins, as well as causing functional changes in neurotransmitter receptors such as nicotinic acetylcholine receptors. Neural activity thus boosts the activity of the dendrite’s satellite micro-secretory system by redistributing Golgi enzymes involved in glycan modifications into peripheral Golgi satellites. This remodeling of the neuronal surface has potential significance for synaptic plasticity, addiction, and disease.Anitha P GovindOkunola JeyifousTheron A RussellZola YiAubrey V WeigelAbhijit RamaprasadLuke NewellWilliam RamosFernando M ValbuenaJason C CaslerJing-Zhi YanBenjamin S GlickGeoffrey T SwansonJennifer Lippincott-SchwartzWilliam N GreeneLife Sciences Publications LtdarticleGolgisialic acidglycosylationnicotineneuronal activityGolgi satellitesMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Golgi sialic acid glycosylation nicotine neuronal activity Golgi satellites Medicine R Science Q Biology (General) QH301-705.5
spellingShingle	Golgi sialic acid glycosylation nicotine neuronal activity Golgi satellites Medicine R Science Q Biology (General) QH301-705.5 Anitha P Govind Okunola Jeyifous Theron A Russell Zola Yi Aubrey V Weigel Abhijit Ramaprasad Luke Newell William Ramos Fernando M Valbuena Jason C Casler Jing-Zhi Yan Benjamin S Glick Geoffrey T Swanson Jennifer Lippincott-Schwartz William N Green Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
description	Activity-driven changes in the neuronal surface glycoproteome are known to occur with synapse formation, plasticity, and related diseases, but their mechanistic basis and significance are unclear. Here, we observed that N-glycans on surface glycoproteins of dendrites shift from immature to mature forms containing sialic acid in response to increased neuronal activation. In exploring the basis of these N-glycosylation alterations, we discovered that they result from the growth and proliferation of Golgi satellites scattered throughout the dendrite. Golgi satellites that formed during neuronal excitation were in close association with endoplasmic reticulum (ER) exit sites and early endosomes and contained glycosylation machinery without the Golgi structural protein, GM130. They functioned as distal glycosylation stations in dendrites, terminally modifying sugars either on newly synthesized glycoproteins passing through the secretory pathway or on surface glycoproteins taken up from the endocytic pathway. These activities led to major changes in the dendritic surface of excited neurons, impacting binding and uptake of lectins, as well as causing functional changes in neurotransmitter receptors such as nicotinic acetylcholine receptors. Neural activity thus boosts the activity of the dendrite’s satellite micro-secretory system by redistributing Golgi enzymes involved in glycan modifications into peripheral Golgi satellites. This remodeling of the neuronal surface has potential significance for synaptic plasticity, addiction, and disease.
format	article
author	Anitha P Govind Okunola Jeyifous Theron A Russell Zola Yi Aubrey V Weigel Abhijit Ramaprasad Luke Newell William Ramos Fernando M Valbuena Jason C Casler Jing-Zhi Yan Benjamin S Glick Geoffrey T Swanson Jennifer Lippincott-Schwartz William N Green
author_facet	Anitha P Govind Okunola Jeyifous Theron A Russell Zola Yi Aubrey V Weigel Abhijit Ramaprasad Luke Newell William Ramos Fernando M Valbuena Jason C Casler Jing-Zhi Yan Benjamin S Glick Geoffrey T Swanson Jennifer Lippincott-Schwartz William N Green
author_sort	Anitha P Govind
title	Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
title_short	Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
title_full	Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
title_fullStr	Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
title_full_unstemmed	Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
title_sort	activity-dependent golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome
publisher	eLife Sciences Publications Ltd
publishDate	2021
url	https://doaj.org/article/00279d88468b4f06978613bb9f77744b
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Activity-dependent Golgi satellite formation in dendrites reshapes the neuronal surface glycoproteome

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