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The Journal of Neuroscience, May 15, 2003, 23(10):4092-4099

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Endocytosis and Vesicle Recycling at a Ribbon Synapse

Christophe Paillart,¹ Jian Li,² Gary Matthews,¹ and Peter Sterling²

¹Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, New York 11794, and ²Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6058

At ribbon synapses, where exocytosis is regulated by graded depolarization, vesicles can fuse very rapidly with the plasma membrane (complete discharge of the releasable pool in 200 msec). Vesicles are also retrieved very rapidly (time constant of 1 sec), leading us to wonder whether their retrieval uses an unusual mechanism. To study this, we exposed isolated bipolar neurons from goldfish retina to cationized ferritin. This electron-dense marker uniformly decorated the cell membrane and was carried into the cell during membrane retrieval. Endocytosis was activity-dependent and restricted to the synaptic terminal. The labeling pattern was consistent with direct retrieval from the plasma membrane of large, uncoated endosomes 60–200 nm in diameter. Even after extensive synaptic activity lasting several minutes, most of the ferritin remained in large endosomes and was present in only 10% of the small vesicles that constitute the reserve pool. By contrast, after brief stimulation at a conventional terminal, ferritin did not reside in endosomes but was present in 63% of the small vesicles. We suggest that the bipolar ribbon synapse sustains its rapid exocytosis by retrieving membrane in larger "bites" than the clathrin-dependent mechanism thought to dominate at conventional synapses. The resulting large endosomes bud off small vesicles, which reenter the reserve pool and finally the releasable pool.

Key words: bipolar cell; transmitter release; goldfish; ferritin tracer; endocytosis; synaptic vesicles

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Received Dec. 10, 2002; revised Feb. 24, 2003; accepted Feb. 25, 2003.

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