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The Journal of Neuroscience, July 15, 2001, 21(14):5169-5181
Stages of Synapse Development Defined by Dependence on F-Actin
Wandong Zhang and Deanna L. Benson Fishberg Research Center for Neurobiology and Program in Cell Adhesion, The Mount Sinai School of Medicine, New York, New York 10029
It has been widely speculated that actin plays a central role in CNS synapse assembly, but such a requirement for actin filaments (F-actin) has not yet been demonstrated experimentally. We used hippocampal neurons grown in culture and the actin depolymerizing agent, latrunculin A, to examine directly the relationship between F-actin and synapse formation and maturation. During the first week in culture, actin depolymerization results in a near complete loss of synapses defined by synaptophysin-labeled vesicle clusters, synaptic vesicle recycling, and ultrastructure. Over the second week in culture, F-actin becomes increasingly stable, but actin depolymerization no longer disrupts basic synaptic structure. There is, however, a reduction in the number and size of synaptophysin-labeled clusters and in the size of vesicle clusters undergoing FM4-64 recycling, suggesting that synaptic vesicle anchoring remains partially dependent on F-actin. By 18 d in culture, synaptophysin clusters and synaptic vesicle recycling are largely resistant to F-actin depolymerization. The decrease in synapse dependence on F-actin correlates well with the acquisition and retention of presynaptic scaffolding proteins such as Bassoon and postsynaptic scaffolding proteins such as those of the postsynaptic density-95 family. Increased activity stabilizes F-actin and its associated proteins at synaptic sites, suggesting a correlation between active synapses, actin stability, and synapse stability. Our findings demonstrate that F-actin is essential for the development and maintenance of young synapses. Because F-actin is also highly regulatable, we propose that F-actin may be a principal target for stabilizing or destabilizing signals that ultimately result in synapse maintenance or elimination.
Key words: actin; presynaptic terminal; postsynaptic density; Bassoon; synaptophysin; tetanus toxin; PSD-95; cadherin; synapse adhesion;
-internexin; dendritic spines
Copyright © 2001 Society for Neuroscience 0270-6474/01/21145169-13$05.00/0
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