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Published online July 9, 2007
doi:10.1083/jcb.200701030
The Journal of Cell Biology, Vol. 178, No. 2, 309-322
The Rockefeller University Press, 0021-9525 $30.00
© 2007 Koh et al.
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Article

 Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development

Tong-Wey Koh1, Viktor I. Korolchuk5, Yogesh P. Wairkar5, Wei Jiao6, Emma Evergren6, Hongling Pan2, Yi Zhou2, Koen J.T. Venken1, Oleg Shupliakov6, Iain M. Robinson5,7, Cahir J. O'Kane5, and Hugo J. Bellen1,2,3,4

1 Graduate Program in Developmental Biology, 2 Department of Molecular and Human Genetics, 3 Department of Neuroscience, and 4 Howard Hughes Medical Institute, Baylor College of Medicine, Houston, TX 77030
5 Department of Genetics, University of Cambridge, Cambridge CB2 3EH, England, UK
6 Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden
7 Institute of Biomedical and Clinical Sciences, Peninsula College of Medicine and Dentistry, Plymouth PL6 8BU, England, UK

Correspondence to Cahir J. O'Kane: c.okane{at}gen.cam.ac.uk; or Hugo J. Bellen: hbellen{at}bcm.tmc.edu

Epidermal growth factor receptor pathway substrate clone 15 (Eps15) is a protein implicated in endocytosis, endosomal protein sorting, and cytoskeletal organization. Its role is, however, still unclear, because of reasons including limitations of dominant-negative experiments and apparent redundancy with other endocytic proteins. We generated Drosophila eps15-null mutants and show that Eps15 is required for proper synaptic bouton development and normal levels of synaptic vesicle (SV) endocytosis. Consistent with a role in SV endocytosis, Eps15 moves from the center of synaptic boutons to the periphery in response to synaptic activity. The endocytic protein, Dap160/intersectin, is a major binding partner of Eps15, and eps15 mutants phenotypically resemble dap160 mutants. Analyses of eps15 dap160 double mutants suggest that Eps15 functions in concert with Dap160 during SV endocytosis. Based on these data, we hypothesize that Eps15 and Dap160 promote the efficiency of endocytosis from the plasma membrane by maintaining high concentrations of multiple endocytic proteins, including dynamin, at synapses.

T.-W. Koh and V.I. Korolchuk contributed equally to this paper.

T.-W. Koh's present address is Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06511.

V.I. Koroluchuk's present address is School of Clinical Medicine, Cambridge Institute for Medical Research, Cambridge CB2 0XY, UK.

Y.P. Wairkar's present address is Department of Molecular Biology and Pharmacology, School of Medicine, Washington University in St. Louis, St. Louis, MO 63110.

Abbreviations used in this paper: Dap160, dynamin-associated protein 160 kD; EH, Eps15 homology; EJP, excitatory junctional potential; Eps15, EGF receptor pathway substrate clone 15; FRT, FLP recognition target; mEJP, miniature EJP; NMJ, neuromuscular junction; SV, synaptic vesicle; TEM, transmission EM; UIM, ubiquitin-interacting motif.


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