Neuroendocrine Synaptic Vesicles Are Formed In Vitro by Both Clathrin-dependent and Clathrin-independent Pathways

doi:10.1083/jcb.143.4.947

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© The Rockefeller University Press, 0021-9525/1998//947 $5.00
The Journal of Cell Biology, Volume 143, Number 4, , 1998 947-955

Regular Articles

Neuroendocrine Synaptic Vesicles Are Formed In Vitro by Both Clathrin-dependent and Clathrin-independent Pathways

Gongyi Shi^*, Victor Faúndez^*, Jack Roos^*, Esteban C. Dell'Angelica, and Regis B. Kelly^*

^* Department of Biochemistry and Biophysics and the Hormone Research Institute, University of California, San Francisco, California 94143-0534; and Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland 20892

In the neuroendocrine cell line, PC12, synaptic vesicles canbe generated from endosomes by a sorting and vesiculation processthat requires the heterotetrameric adaptor protein AP3 and asmall molecular weight GTPase of the ADP ribosylation factor(ARF) family. We have now discovered a second pathway that sorts the synaptic vesicle-associated membrane protein (VAMP)into similarly sized vesicles. For this pathway the plasmamembrane is the precursor rather than endosomes. Both pathwaysrequire cytosol and ATP and are inhibited by GTP ${gamma}$ S. The secondpathway, however, uses AP2 instead of AP3 and is brefeldinA insensitive. The AP2-dependent pathway is inhibited by depletion of clathrin or by inhibitors of clathrin binding, whereas the AP3 pathway is not. The VAMP-containing, plasma membrane–derivedvesicles can be readily separated on sucrose gradients fromtransferrin (Tf)-containing vesicles generated by incubatingTf-labeled plasma membrane preparations at 37°C. Dynamin-interacting proteins are required for the AP2-mediated vesiculationfrom the plasma membrane, but not from endosomes. Thus, VAMPis sorted into small vesicles by AP3 and ARF1 at endosomesand by AP2 and clathrin at the plasma membrane.

Key Words: synaptic vesicles • clathrin • plasma membrane • PC12 cells • VAMP

Abbreviations used in this paper: AP, adaptor protein; ARF, ADP ribosylation factor; BFA, brefeldin A; PRD, proline-rich domain; SV, synaptic vesicle; TAg, T antigen; Tf, transferrin; TfR, transferrin receptor; VAMP, vesicle-associated membrane protein.

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