Presynaptic morphology and vesicular composition determine vesicle dynamics in mouse central synapses

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Cite this article as: eLife 2017;6:e24845 doi: 10.7554/eLife.24845

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Abstract

Transport of synaptic vesicles (SVs) in nerve terminals is thought to play essential roles in maintenance of neurotransmission. To identify factors modulating SV movements, we performed real-time imaging analysis of fluorescently labeled SVs in giant calyceal and conventional hippocampal terminals. Compared with small hippocampal terminals, SV movements in giant calyceal terminals were faster, longer and kinetically more heterogeneous. Morphological maturation of giant calyceal terminals was associated with an overall reduction in SV mobility and displacement heterogeneity. At the molecular level, SVs over-expressing vesicular glutamate transporter 1 (VGLUT1) showed higher mobility than VGLUT2-expressing SVs. Pharmacological disruption of the presynaptic microtubule network preferentially reduced long directional movements of SVs between release sites. Functionally, synaptic stimulation appeared to recruit SVs to active zones without significantly altering their mobility. Hence, the morphological features of nerve terminals and the molecular signature of vesicles are key elements determining vesicular dynamics and movements in central synapses.

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Author details

Laurent Guillaud

Cellular and Molecular Synaptic Function Unit, Okinawa Institute of Science and Technology - Graduate University, Onna, Japan

For correspondence
laurent.guillaud@oist.jp

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9688-0991
Dimitar Dimitrov

Cellular and Molecular Synaptic Function Unit, Okinawa Institute of Science and Technology - Graduate University, Onna, Japan

Competing interests
The authors declare that no competing interests exist.
Tomoyuki Takahashi

Cellular and Molecular Synaptic Function Unit, Okinawa Institute of Science and Technology - Graduate University, Onna, Japan

For correspondence
ttakahas@oist.jp

Competing interests
The authors declare that no competing interests exist.

Funding

Okinawa Institute of Science and Technology Graduate University

Tomoyuki Takahashi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments have been performed in accordance to the regulations of OIST animal care and use committee (protocol #2015-128). OIST animal facilities and animal care and use program are accredited by AAALAC International (reference #1551).

Reviewing Editor

Christian Rosenmund, Charité-Universitätsmedizin Berlin, Germany

Publication history

Received: January 2, 2017
Accepted: April 18, 2017
Accepted Manuscript published: April 22, 2017 (version 1)
Version of Record published: May 9, 2017 (version 2)
Version of Record updated: May 12, 2017 (version 3)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.