Formation of presynaptic terminals at predefined sites along axons

Shasta L. Sabo, Raquel A. Gomes, A Kimberley Usrey

Research output: Contribution to journalArticle

87 Citations (Scopus)

Abstract

What determines where synapses will form along an axon or how proteins are deposited at nascent synapses remains unknown. Here, we show that the initial formation of presynaptic terminals occurs preferentially at predefined sites within the axons of cortical neurons. Time-lapse imaging of synaptic vesicle protein transport vesicles (STVs) indicates that STVs pause repeatedly at these sites, even in the absence of neuronal or glial contact. Contact with a neuroligin-expressing non-neuronal cell induces formation of presynaptic terminals specifically at these STV pause sites. Remarkably, formation of stable contacts with dendritic filopodia also occurs selectively at STV pause sites. Although it is not yet known which molecules comprise the predefined sites, STV pausing is regulated by cues that affect synaptogenesis. Overall, these data are consistent with the hypothesis that regulation of STV pausing might be an important mechanism for accumulation of presynaptic proteins at nascent synapses and support a new model in which many en passant synapses form specifically at predefined sites in young axons.

Original languageEnglish (US)
Pages (from-to)10813-10825
Number of pages13
JournalJournal of Neuroscience
Volume26
Issue number42
DOIs
StatePublished - Oct 18 2006

Fingerprint

Transport Vesicles
Synaptic Vesicles
Presynaptic Terminals
Protein Transport
Axons
Synapses
Time-Lapse Imaging
Pseudopodia
Neuroglia
Cues
Proteins
Neurons

Keywords

  • Development
  • Synapse formation
  • Synaptogenesis
  • Time-lapse imaging
  • VAMP-EGFP
  • Visual cortex

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Formation of presynaptic terminals at predefined sites along axons. / Sabo, Shasta L.; Gomes, Raquel A.; Usrey, A Kimberley.

In: Journal of Neuroscience, Vol. 26, No. 42, 18.10.2006, p. 10813-10825.

Research output: Contribution to journalArticle

Sabo, Shasta L. ; Gomes, Raquel A. ; Usrey, A Kimberley. / Formation of presynaptic terminals at predefined sites along axons. In: Journal of Neuroscience. 2006 ; Vol. 26, No. 42. pp. 10813-10825.
@article{34917f730baf4e4ca069aa2ee06a204e,
title = "Formation of presynaptic terminals at predefined sites along axons",
abstract = "What determines where synapses will form along an axon or how proteins are deposited at nascent synapses remains unknown. Here, we show that the initial formation of presynaptic terminals occurs preferentially at predefined sites within the axons of cortical neurons. Time-lapse imaging of synaptic vesicle protein transport vesicles (STVs) indicates that STVs pause repeatedly at these sites, even in the absence of neuronal or glial contact. Contact with a neuroligin-expressing non-neuronal cell induces formation of presynaptic terminals specifically at these STV pause sites. Remarkably, formation of stable contacts with dendritic filopodia also occurs selectively at STV pause sites. Although it is not yet known which molecules comprise the predefined sites, STV pausing is regulated by cues that affect synaptogenesis. Overall, these data are consistent with the hypothesis that regulation of STV pausing might be an important mechanism for accumulation of presynaptic proteins at nascent synapses and support a new model in which many en passant synapses form specifically at predefined sites in young axons.",
keywords = "Development, Synapse formation, Synaptogenesis, Time-lapse imaging, VAMP-EGFP, Visual cortex",
author = "Sabo, {Shasta L.} and Gomes, {Raquel A.} and Usrey, {A Kimberley}",
year = "2006",
month = "10",
day = "18",
doi = "10.1523/JNEUROSCI.2052-06.2006",
language = "English (US)",
volume = "26",
pages = "10813--10825",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "42",

}

TY - JOUR

T1 - Formation of presynaptic terminals at predefined sites along axons

AU - Sabo, Shasta L.

AU - Gomes, Raquel A.

AU - Usrey, A Kimberley

PY - 2006/10/18

Y1 - 2006/10/18

N2 - What determines where synapses will form along an axon or how proteins are deposited at nascent synapses remains unknown. Here, we show that the initial formation of presynaptic terminals occurs preferentially at predefined sites within the axons of cortical neurons. Time-lapse imaging of synaptic vesicle protein transport vesicles (STVs) indicates that STVs pause repeatedly at these sites, even in the absence of neuronal or glial contact. Contact with a neuroligin-expressing non-neuronal cell induces formation of presynaptic terminals specifically at these STV pause sites. Remarkably, formation of stable contacts with dendritic filopodia also occurs selectively at STV pause sites. Although it is not yet known which molecules comprise the predefined sites, STV pausing is regulated by cues that affect synaptogenesis. Overall, these data are consistent with the hypothesis that regulation of STV pausing might be an important mechanism for accumulation of presynaptic proteins at nascent synapses and support a new model in which many en passant synapses form specifically at predefined sites in young axons.

AB - What determines where synapses will form along an axon or how proteins are deposited at nascent synapses remains unknown. Here, we show that the initial formation of presynaptic terminals occurs preferentially at predefined sites within the axons of cortical neurons. Time-lapse imaging of synaptic vesicle protein transport vesicles (STVs) indicates that STVs pause repeatedly at these sites, even in the absence of neuronal or glial contact. Contact with a neuroligin-expressing non-neuronal cell induces formation of presynaptic terminals specifically at these STV pause sites. Remarkably, formation of stable contacts with dendritic filopodia also occurs selectively at STV pause sites. Although it is not yet known which molecules comprise the predefined sites, STV pausing is regulated by cues that affect synaptogenesis. Overall, these data are consistent with the hypothesis that regulation of STV pausing might be an important mechanism for accumulation of presynaptic proteins at nascent synapses and support a new model in which many en passant synapses form specifically at predefined sites in young axons.

KW - Development

KW - Synapse formation

KW - Synaptogenesis

KW - Time-lapse imaging

KW - VAMP-EGFP

KW - Visual cortex

UR - http://www.scopus.com/inward/record.url?scp=33750951076&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33750951076&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.2052-06.2006

DO - 10.1523/JNEUROSCI.2052-06.2006

M3 - Article

C2 - 17050720

AN - SCOPUS:33750951076

VL - 26

SP - 10813

EP - 10825

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 42

ER -