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Published online 19 May 2003. doi:10.1083/jcb.200212140
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© The Rockefeller University Press, 0021-9525/2003/5/737 $5.00
The Journal of Cell Biology, Volume 161, Number 4, 737-747

Article

Colocalization of synapsin and actin during synaptic vesicle recycling



Ona Bloom1,2, Emma Evergren2, Nikolay Tomilin2, Ole Kjaerulff2, Peter Löw2, Lennart Brodin2, Vincent A. Pieribone1, Paul Greengard1 and Oleg Shupliakov2

1 Laboratory of Molecular and Cellular Neuroscience, The Rockefeller University, New York, NY 10021
2 Center of Excellence in Developmental Biology, Department of Neuroscience, Karolinska Institutet, S-171 77, Stockholm, Sweden

Address correspondence to Ona Bloom, Department of Cell Biology, Yale University School of Medicine, P.O. Box 208002, New Haven, CT 06520. Tel.: (203) 785-6078. Fax: (203) 785-4301. E-mail: ona{at}chronos.med.yale.edu; or Oleg Shupliakov, Department of Neuroscience, CED8 Karolinska Institutet, S-171 77, Stockholm, Sweden. Tel.: (468) 7287849. Fax: (468) 325861. E-mail: oleg.shupliakov{at}neuro.ki.se

It has been hypothesized that in the mature nerve terminal, interactions between synapsin and actin regulate the clustering of synaptic vesicles and the availability of vesicles for release during synaptic activity. Here, we have used immunogold electron microscopy to examine the subcellular localization of actin and synapsin in the giant synapse in lamprey at different states of synaptic activity. In agreement with earlier observations, in synapses at rest, synapsin immunoreactivity was preferentially localized to a portion of the vesicle cluster distal to the active zone. During synaptic activity, however, synapsin was detected in the pool of vesicles proximal to the active zone. In addition, actin and synapsin were found colocalized in a dynamic filamentous cytomatrix at the sites of synaptic vesicle recycling, endocytic zones. Synapsin immunolabeling was not associated with clathrin-coated intermediates but was found on vesicles that appeared to be recycling back to the cluster. Disruption of synapsin function by microinjection of antisynapsin antibodies resulted in a prominent reduction of the cytomatrix at endocytic zones of active synapses. Our data suggest that in addition to its known function in clustering of vesicles in the reserve pool, synapsin migrates from the synaptic vesicle cluster and participates in the organization of the actin-rich cytomatrix in the endocytic zone during synaptic activity.

Key Words: synapsin; actin; synapse; neurotransmission; endocytosis

O. Bloom's present address is Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06520.

O. Kjaerulff's present address is Institute of Medical Physiology, Copenhagen University, Blegdamsvej 3, DK-2200, Copenhagen, Denmark.

V.A. Pieribone's present address is The John B. Pierce Laboratory, Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06519.

* Abbreviations used in this paper: 3-D, three-dimensional; CaMKII, calmodulin-dependent protein kinase II; F-actin, filamentous actin; G-actin, globular actin; SV2, synaptic vesicle protein 2.


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