β-Catenin regulates excitatory postsynaptic strength at hippocampal synapses

Takashi Okuda, Lily M Y Yu, Lorenzo A. Cingolani, Rolf Kemler, Yukiko Goda

Research output: Contribution to journalArticle

94 Citations (Scopus)

Abstract

The precise contribution of the cadherin-β-catenin synapse adhesion complex in the functional and structural changes associated with the pre- and postsynaptic terminals remains unclear. Here we report a requirement for endogenous β-catenin in regulating synaptic strength and dendritic spine morphology in cultured hippocampal pyramidal neurons. Ablating β-catenin after the initiation of synaptogenesis in the postsynaptic neuron reduces the amplitude of spontaneous excitatory synaptic responses without a concurrent change in their frequency and synapse density. The normal glutamatergic synaptic response is maintained by postsynaptic β-catenin in a cadherin-dependent manner and requires the C-terminal PDZ-binding motif of β-catenin but not the link to the actin cytoskeleton. In addition, ablating β-catenin in postsynaptic neurons accompanies a block of bidirectional quantal scaling of glutamatergic responses induced by chronic activity manipulation. In older cultures at a time when neurons have abundant dendritic spines, neurons ablated for β-catenin show thin, elongated spines and reduced proportion of mushroom spines without a change in spine density. Collectively, these findings suggest that the cadherin-β-catenin complex is an integral component of synaptic strength regulation and plays a basic role in coupling synapse function and spine morphology.

Original languageEnglish
Pages (from-to)13479-13484
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume104
Issue number33
DOIs
Publication statusPublished - 2007 Aug 14
Externally publishedYes

Fingerprint

Catenins
Synapses
Spine
Cadherins
Neurons
Dendritic Spines
Pyramidal Cells
Agaricales
Presynaptic Terminals
Actin Cytoskeleton

Keywords

  • α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors
  • Quantal scaling
  • Spine morphology
  • Synapse adhesion proteins

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

β-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. / Okuda, Takashi; Yu, Lily M Y; Cingolani, Lorenzo A.; Kemler, Rolf; Goda, Yukiko.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 104, No. 33, 14.08.2007, p. 13479-13484.

Research output: Contribution to journalArticle

Okuda, Takashi ; Yu, Lily M Y ; Cingolani, Lorenzo A. ; Kemler, Rolf ; Goda, Yukiko. / β-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. In: Proceedings of the National Academy of Sciences of the United States of America. 2007 ; Vol. 104, No. 33. pp. 13479-13484.
@article{0a1c3b9869ab474aa056bfb7f4f3cb48,
title = "β-Catenin regulates excitatory postsynaptic strength at hippocampal synapses",
abstract = "The precise contribution of the cadherin-β-catenin synapse adhesion complex in the functional and structural changes associated with the pre- and postsynaptic terminals remains unclear. Here we report a requirement for endogenous β-catenin in regulating synaptic strength and dendritic spine morphology in cultured hippocampal pyramidal neurons. Ablating β-catenin after the initiation of synaptogenesis in the postsynaptic neuron reduces the amplitude of spontaneous excitatory synaptic responses without a concurrent change in their frequency and synapse density. The normal glutamatergic synaptic response is maintained by postsynaptic β-catenin in a cadherin-dependent manner and requires the C-terminal PDZ-binding motif of β-catenin but not the link to the actin cytoskeleton. In addition, ablating β-catenin in postsynaptic neurons accompanies a block of bidirectional quantal scaling of glutamatergic responses induced by chronic activity manipulation. In older cultures at a time when neurons have abundant dendritic spines, neurons ablated for β-catenin show thin, elongated spines and reduced proportion of mushroom spines without a change in spine density. Collectively, these findings suggest that the cadherin-β-catenin complex is an integral component of synaptic strength regulation and plays a basic role in coupling synapse function and spine morphology.",
keywords = "α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors, Quantal scaling, Spine morphology, Synapse adhesion proteins",
author = "Takashi Okuda and Yu, {Lily M Y} and Cingolani, {Lorenzo A.} and Rolf Kemler and Yukiko Goda",
year = "2007",
month = "8",
day = "14",
doi = "10.1073/pnas.0702334104",
language = "English",
volume = "104",
pages = "13479--13484",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "33",

}

TY - JOUR

T1 - β-Catenin regulates excitatory postsynaptic strength at hippocampal synapses

AU - Okuda, Takashi

AU - Yu, Lily M Y

AU - Cingolani, Lorenzo A.

AU - Kemler, Rolf

AU - Goda, Yukiko

PY - 2007/8/14

Y1 - 2007/8/14

N2 - The precise contribution of the cadherin-β-catenin synapse adhesion complex in the functional and structural changes associated with the pre- and postsynaptic terminals remains unclear. Here we report a requirement for endogenous β-catenin in regulating synaptic strength and dendritic spine morphology in cultured hippocampal pyramidal neurons. Ablating β-catenin after the initiation of synaptogenesis in the postsynaptic neuron reduces the amplitude of spontaneous excitatory synaptic responses without a concurrent change in their frequency and synapse density. The normal glutamatergic synaptic response is maintained by postsynaptic β-catenin in a cadherin-dependent manner and requires the C-terminal PDZ-binding motif of β-catenin but not the link to the actin cytoskeleton. In addition, ablating β-catenin in postsynaptic neurons accompanies a block of bidirectional quantal scaling of glutamatergic responses induced by chronic activity manipulation. In older cultures at a time when neurons have abundant dendritic spines, neurons ablated for β-catenin show thin, elongated spines and reduced proportion of mushroom spines without a change in spine density. Collectively, these findings suggest that the cadherin-β-catenin complex is an integral component of synaptic strength regulation and plays a basic role in coupling synapse function and spine morphology.

AB - The precise contribution of the cadherin-β-catenin synapse adhesion complex in the functional and structural changes associated with the pre- and postsynaptic terminals remains unclear. Here we report a requirement for endogenous β-catenin in regulating synaptic strength and dendritic spine morphology in cultured hippocampal pyramidal neurons. Ablating β-catenin after the initiation of synaptogenesis in the postsynaptic neuron reduces the amplitude of spontaneous excitatory synaptic responses without a concurrent change in their frequency and synapse density. The normal glutamatergic synaptic response is maintained by postsynaptic β-catenin in a cadherin-dependent manner and requires the C-terminal PDZ-binding motif of β-catenin but not the link to the actin cytoskeleton. In addition, ablating β-catenin in postsynaptic neurons accompanies a block of bidirectional quantal scaling of glutamatergic responses induced by chronic activity manipulation. In older cultures at a time when neurons have abundant dendritic spines, neurons ablated for β-catenin show thin, elongated spines and reduced proportion of mushroom spines without a change in spine density. Collectively, these findings suggest that the cadherin-β-catenin complex is an integral component of synaptic strength regulation and plays a basic role in coupling synapse function and spine morphology.

KW - α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors

KW - Quantal scaling

KW - Spine morphology

KW - Synapse adhesion proteins

UR - http://www.scopus.com/inward/record.url?scp=34548058077&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34548058077&partnerID=8YFLogxK

U2 - 10.1073/pnas.0702334104

DO - 10.1073/pnas.0702334104

M3 - Article

C2 - 17679699

AN - SCOPUS:34548058077

VL - 104

SP - 13479

EP - 13484

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 33

ER -