Cadherin activity is required for activity-induced spine remodeling

Neural activity induces the remodeling of pre- and postsynaptic membranes, which maintain their apposition through cell adhesion molecules. Among them, N-cadherin is redistributed, undergoes activity-dependent conformational changes, and is required for synaptic plasticity. Here, we show that depolarization induces the enlargement of the width of spine head, and that cadherin activity is essential for this synaptic rearrangement. Dendritic spines visualized with green fluorescent protein in hippocampal neurons showed an expansion by the activation of AMPA receptor, so that the synaptic apposition zone may be expanded. N-cadherin-venus fusion protein laterally dispersed along the expanding spine head. Overexpression of dominant-negative forms of N-cadherin resulted in the abrogation of the spine expansion. Inhibition of actin polymerization with cytochalasin D abolished the spine expansion. Together, our data suggest that cadherin-based adhesion machinery coupled with the actin-cytoskeleton is critical for the remodeling of synaptic apposition zone.

[1]  B. Gähwiler,et al.  AMPA‐receptor activation regulates the diffusion of a membrane marker in parallel with dendritic spine motility in the mouse hippocampus , 2004, The Journal of physiology.

[2]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[3]  M. Takeichi,et al.  Stability of dendritic spines and synaptic contacts is controlled by αN-catenin , 2004, Nature Neuroscience.

[4]  W. Birchmeier,et al.  Role of β-Catenin in Synaptic Vesicle Localization and Presynaptic Assembly , 2003, Neuron.

[5]  A. Fine,et al.  Imaging spatio-temporal patterns of long-term potentiation in mouse hippocampus. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  S. Narumiya,et al.  Multiple spatiotemporal modes of actin reorganization by NMDA receptors and voltage-gated Ca2+ channels , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Fiala,et al.  Polyribosomes Redistribute from Dendritic Shafts into Spines with Enlarged Synapses during LTP in Developing Rat Hippocampal Slices , 2002, Neuron.

[8]  M. Takeichi,et al.  Cadherin Regulates Dendritic Spine Morphogenesis , 2002, Neuron.

[9]  E. Schuman,et al.  Depolarization Drives β-Catenin into Neuronal Spines Promoting Changes in Synaptic Structure and Function , 2002, Neuron.

[10]  O. Prange,et al.  Modular Transport of Postsynaptic Density-95 Clusters and Association with Stable Spine Precursors during Early Development of Cortical Neurons , 2001, The Journal of Neuroscience.

[11]  Michael J. Sailor,et al.  Remodeling of Synaptic Actin Induced by Photoconductive Stimulation , 2001, Cell.

[12]  Yingming Zhao,et al.  The Presynaptic Particle Web Ultrastructure, Composition, Dissolution, and Reconstitution , 2001, Neuron.

[13]  D. Benson,et al.  Stages of Synapse Development Defined by Dependence on F-Actin , 2001, The Journal of Neuroscience.

[14]  R. Yuste,et al.  Regulation of Spine Calcium Dynamics by Rapid Spine Motility Materials and Methods , 2022 .

[15]  O. Bozdagi,et al.  Increasing Numbers of Synaptic Puncta during Late-Phase LTP N-Cadherin Is Synthesized, Recruited to Synaptic Sites, and Required for Potentiation , 2000, Neuron.

[16]  M. Fischer,et al.  Glutamate receptors regulate actin-based plasticity in dendritic spines , 2000, Nature Neuroscience.

[17]  T. Manabe,et al.  Loss of Cadherin-11 Adhesion Receptor Enhances Plastic Changes in Hippocampal Synapses and Modifies Behavioral Responses , 2000, Molecular and Cellular Neuroscience.

[18]  L. Shapiro,et al.  Functional Cis-Heterodimers of N- and R-Cadherins , 2000, The Journal of cell biology.

[19]  David R. Colman,et al.  Molecular Modification of N-Cadherin in Response to Synaptic Activity , 2000, Neuron.

[20]  N. Toni,et al.  LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite , 1999, Nature.

[21]  M Segal,et al.  Release of calcium from stores alters the morphology of dendritic spines in cultured hippocampal neurons. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Y. Hiraoka,et al.  Multiple-color fluorescence imaging of chromosomes and microtubules in living cells. , 1999, Cell structure and function.

[23]  P. Worley,et al.  Arcadlin Is a Neural Activity-regulated Cadherin Involved in Long Term Potentiation* , 1999, The Journal of Biological Chemistry.

[24]  K. Svoboda,et al.  Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. , 1999, Science.

[25]  J. Sanes,et al.  Expression of Multiple Cadherins and Catenins in the Chick Optic Tectum , 1998, Molecular and Cellular Neuroscience.

[26]  Hidekazu Tanaka,et al.  N-Cadherin Redistribution during Synaptogenesis in Hippocampal Neurons , 1998, The Journal of Neuroscience.

[27]  Wayne A. Hendrickson,et al.  Structure-Function Analysis of Cell Adhesion by Neural (N-) Cadherin , 1998, Neuron.

[28]  Chou P Hung,et al.  A Role for the Cadherin Family of Cell Adhesion Molecules in Hippocampal Long-Term Potentiation , 1998, Neuron.

[29]  M. Fischer,et al.  Rapid Actin-Based Plasticity in Dendritic Spines , 1998, Neuron.

[30]  Takayoshi Inoue,et al.  Cadherin‐6 in the developing mouse brain: Expression along restricted connection systems and synaptic localization suggest a potential role in neuronal circuitry , 1998, Developmental dynamics : an official publication of the American Association of Anatomists.

[31]  M. Takeichi,et al.  The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones , 1996, The Journal of cell biology.

[32]  D. Colman,et al.  A Model for Central Synaptic Junctional Complex Formation Based on the Differential Adhesive Specificities of the Cadherins , 1996, Neuron.

[33]  D. Muller,et al.  Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[34]  M. Yamagata,et al.  Lamina-specific expression of adhesion molecules in developing chick optic tectum , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  P. McCrea,et al.  Catenins as mediators of the cytoplasmic functions of cadherins , 1993, Journal of Cell Science.

[36]  C. Kintner.  Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain , 1992, Cell.

[37]  Leyla deToledo-Morrell,et al.  Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities , 1991, Brain Research.

[38]  C. Stevens,et al.  NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus , 1989, Nature.

[39]  M. Takeichi,et al.  Functional correlation between cell adhesive properties and some cell surface proteins , 1977, The Journal of cell biology.

[40]  M. Takeichi,et al.  Stability of dendritic spines and synaptic contacts is controlled by alpha N-catenin. , 2004, Nature neuroscience.

[41]  W. Birchmeier,et al.  Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. , 2003, Neuron.

[42]  K. Mikoshiba,et al.  A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications , 2002, Nature Biotechnology.

[43]  M. Takeichi,et al.  Cadherins: a molecular family important in selective cell-cell adhesion. , 1990, Annual review of biochemistry.

[44]  D. Agard,et al.  Fluorescence microscopy in three dimensions. , 1989, Methods in cell biology.