The function of p120 catenin in filopodial growth and synaptic vesicle clustering in neurons

Cheng Chen, Pan Li, Raghavan Madhavan, H. Benjamin Peng

Research output: Contribution to journalArticle

Abstract

At the developing neuromuscular junction (NMJ), physical contact between motor axons and muscle cells initiates presynaptic and postsynaptic differentiation. Using Xenopus nerve-muscle cocultures, we previously showed that innervating axons induced muscle filopodia (myopodia), which facilitated interactions between the synaptic partners and promoted NMJ formation. The myopodia were generated by nerve-released signals through muscle p120 catenin (p120ctn), a protein of the cadherin complex that modulates the activity of Rho GTPases. Because axons also extend filopodia that mediate early nerve-muscle interactions, here we test p120ctn's function in the assembly of these presynaptic processes. Overexpression of wild-type p120ctn in Xenopus spinal neurons leads to an increase in filopodial growth and synaptic vesicle (SV) clustering along axons, whereas the development of these specializations is inhibited following the expression of a p120ctn mutant lacking sequences important for regulating Rho GTPases. The p120ctn mutant also inhibits the induction of axonal filopodia and SV clusters by basic fibroblast growth factor, a muscle-derived molecule that triggers presynaptic differentiation. Of importance, introduction of the p120ctn mutant into neurons hinders NMJ formation, which is observed as a reduction in the accumulation of acetylcholine receptors at innervation sites in muscle. Our results suggest that p120ctn signaling in motor neurons promotes nerve-muscle interaction and NMJ assembly.

Original languageEnglish (US)
Pages (from-to)2680-2691
Number of pages12
JournalMolecular Biology of the Cell
Volume23
Issue number14
DOIs
StatePublished - Jul 15 2012
Externally publishedYes

Fingerprint

Synaptic Vesicles
Cluster Analysis
Neuromuscular Junction
Neurons
Muscles
Pseudopodia
Growth
Axons
rho GTP-Binding Proteins
Xenopus
Motor Neurons
Cholinergic Receptors
Fibroblast Growth Factor 2
Cadherins
Coculture Techniques
delta catenin
Muscle Cells

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

The function of p120 catenin in filopodial growth and synaptic vesicle clustering in neurons. / Chen, Cheng; Li, Pan; Madhavan, Raghavan; Peng, H. Benjamin.

In: Molecular Biology of the Cell, Vol. 23, No. 14, 15.07.2012, p. 2680-2691.

Research output: Contribution to journalArticle

Chen, Cheng ; Li, Pan ; Madhavan, Raghavan ; Peng, H. Benjamin. / The function of p120 catenin in filopodial growth and synaptic vesicle clustering in neurons. In: Molecular Biology of the Cell. 2012 ; Vol. 23, No. 14. pp. 2680-2691.
@article{396fb3faac114fef96ec5d614944016b,
title = "The function of p120 catenin in filopodial growth and synaptic vesicle clustering in neurons",
abstract = "At the developing neuromuscular junction (NMJ), physical contact between motor axons and muscle cells initiates presynaptic and postsynaptic differentiation. Using Xenopus nerve-muscle cocultures, we previously showed that innervating axons induced muscle filopodia (myopodia), which facilitated interactions between the synaptic partners and promoted NMJ formation. The myopodia were generated by nerve-released signals through muscle p120 catenin (p120ctn), a protein of the cadherin complex that modulates the activity of Rho GTPases. Because axons also extend filopodia that mediate early nerve-muscle interactions, here we test p120ctn's function in the assembly of these presynaptic processes. Overexpression of wild-type p120ctn in Xenopus spinal neurons leads to an increase in filopodial growth and synaptic vesicle (SV) clustering along axons, whereas the development of these specializations is inhibited following the expression of a p120ctn mutant lacking sequences important for regulating Rho GTPases. The p120ctn mutant also inhibits the induction of axonal filopodia and SV clusters by basic fibroblast growth factor, a muscle-derived molecule that triggers presynaptic differentiation. Of importance, introduction of the p120ctn mutant into neurons hinders NMJ formation, which is observed as a reduction in the accumulation of acetylcholine receptors at innervation sites in muscle. Our results suggest that p120ctn signaling in motor neurons promotes nerve-muscle interaction and NMJ assembly.",
author = "Cheng Chen and Pan Li and Raghavan Madhavan and Peng, {H. Benjamin}",
year = "2012",
month = "7",
day = "15",
doi = "10.1091/mbc.E12-01-0004",
language = "English (US)",
volume = "23",
pages = "2680--2691",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "14",

}

TY - JOUR

T1 - The function of p120 catenin in filopodial growth and synaptic vesicle clustering in neurons

AU - Chen, Cheng

AU - Li, Pan

AU - Madhavan, Raghavan

AU - Peng, H. Benjamin

PY - 2012/7/15

Y1 - 2012/7/15

N2 - At the developing neuromuscular junction (NMJ), physical contact between motor axons and muscle cells initiates presynaptic and postsynaptic differentiation. Using Xenopus nerve-muscle cocultures, we previously showed that innervating axons induced muscle filopodia (myopodia), which facilitated interactions between the synaptic partners and promoted NMJ formation. The myopodia were generated by nerve-released signals through muscle p120 catenin (p120ctn), a protein of the cadherin complex that modulates the activity of Rho GTPases. Because axons also extend filopodia that mediate early nerve-muscle interactions, here we test p120ctn's function in the assembly of these presynaptic processes. Overexpression of wild-type p120ctn in Xenopus spinal neurons leads to an increase in filopodial growth and synaptic vesicle (SV) clustering along axons, whereas the development of these specializations is inhibited following the expression of a p120ctn mutant lacking sequences important for regulating Rho GTPases. The p120ctn mutant also inhibits the induction of axonal filopodia and SV clusters by basic fibroblast growth factor, a muscle-derived molecule that triggers presynaptic differentiation. Of importance, introduction of the p120ctn mutant into neurons hinders NMJ formation, which is observed as a reduction in the accumulation of acetylcholine receptors at innervation sites in muscle. Our results suggest that p120ctn signaling in motor neurons promotes nerve-muscle interaction and NMJ assembly.

AB - At the developing neuromuscular junction (NMJ), physical contact between motor axons and muscle cells initiates presynaptic and postsynaptic differentiation. Using Xenopus nerve-muscle cocultures, we previously showed that innervating axons induced muscle filopodia (myopodia), which facilitated interactions between the synaptic partners and promoted NMJ formation. The myopodia were generated by nerve-released signals through muscle p120 catenin (p120ctn), a protein of the cadherin complex that modulates the activity of Rho GTPases. Because axons also extend filopodia that mediate early nerve-muscle interactions, here we test p120ctn's function in the assembly of these presynaptic processes. Overexpression of wild-type p120ctn in Xenopus spinal neurons leads to an increase in filopodial growth and synaptic vesicle (SV) clustering along axons, whereas the development of these specializations is inhibited following the expression of a p120ctn mutant lacking sequences important for regulating Rho GTPases. The p120ctn mutant also inhibits the induction of axonal filopodia and SV clusters by basic fibroblast growth factor, a muscle-derived molecule that triggers presynaptic differentiation. Of importance, introduction of the p120ctn mutant into neurons hinders NMJ formation, which is observed as a reduction in the accumulation of acetylcholine receptors at innervation sites in muscle. Our results suggest that p120ctn signaling in motor neurons promotes nerve-muscle interaction and NMJ assembly.

UR - http://www.scopus.com/inward/record.url?scp=84863947356&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84863947356&partnerID=8YFLogxK

U2 - 10.1091/mbc.E12-01-0004

DO - 10.1091/mbc.E12-01-0004

M3 - Article

C2 - 22648172

AN - SCOPUS:84863947356

VL - 23

SP - 2680

EP - 2691

JO - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 14

ER -