Golgi-independent secretory trafficking through recycling endosomes in neuronal dendrites and spines

Neurons face the challenge of regulating the abundance, distribution and repertoire of integral membrane proteins within their immense, architecturally complex dendritic arbors. While the endoplasmic reticulum (ER) supports dendritic translation, most dendrites lack the Golgi apparatus (GA), an esse...

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Bibliographic Details
Published in:eLife 2017-09, Vol.6
Main Authors: Bowen, Aaron B, Bourke, Ashley M, Hiester, Brian G, Hanus, Cyril, Kennedy, Matthew J
Format: Article
Language:English
Subjects:
AMPA receptor
Animals
Brain
Cell adhesion & migration
Cell Adhesion Molecules, Neuronal - metabolism
Cell Biology
Cell membranes
Cerebral Cortex - physiology
Dendrites - metabolism
Dendritic spines
Diseases
Endoplasmic reticulum
Endosomes
Endosomes - metabolism
Enzymes
Glutamate
Glutamic acid receptors
Golgi apparatus
Membrane proteins
Microscopy
Neurons
Neuroscience
Protein Transport
Protein turnover
Proteins
Rats
Receptors, AMPA - metabolism
recycling endosome
Rodents
secretory network
secretory trafficking
Statistical analysis
synapse
Time
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
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Summary:Neurons face the challenge of regulating the abundance, distribution and repertoire of integral membrane proteins within their immense, architecturally complex dendritic arbors. While the endoplasmic reticulum (ER) supports dendritic translation, most dendrites lack the Golgi apparatus (GA), an essential organelle for conventional secretory trafficking. Thus, whether secretory cargo is locally trafficked in dendrites through a non-canonical pathway remains a fundamental question. Here we define the dendritic trafficking itinerary for key synaptic molecules in rat cortical neurons. Following ER exit, the AMPA-type glutamate receptor GluA1 and neuroligin 1 undergo spatially restricted entry into the dendritic secretory pathway and accumulate in recycling endosomes (REs) located in dendrites and spines before reaching the plasma membrane. Surprisingly, GluA1 surface delivery occurred even when GA function was disrupted. Thus, in addition to their canonical role in protein recycling, REs also mediate forward secretory trafficking in neuronal dendrites and spines through a specialized GA-independent trafficking network.
ISSN:2050-084X
2050-084X
DOI:10.7554/elife.27362