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Published 7 July 2003. doi:10.1083/jcb.200301006
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© The Rockefeller University Press, 0021-9525/2003/7/113 $5.00
The Journal of Cell Biology, Volume 162, Number 1, 113-124

Article

ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type I{gamma}



Michael Krauss1, Masahiro Kinuta2, Markus R. Wenk3, Pietro De Camilli3, Kohji Takei2 and Volker Haucke1

1 Department of Biochemistry II, Zentrum für Biochemie und Molekulare Zellbiologie, University of Göttingen, D-37073 Göttingen, Germany
2 Department of Neuroscience, Okayama University Graduate School of Medicine and Dentistry, Okayama 700-8558, Japan
3 Department of Cell Biology and Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT 06510

Address correspondence to Volker Haucke, Zentrum für Biochemie und Molekulare Zellbiologie, Dept. of Biochemistry II, University of Göttingen, Humboldtallee 23, Göttingen D-37073, Germany. Tel.: 49-551-39-98-54. Fax: 49-551-39-12-198. E-mail: vhaucke{at}gwdg.de

Clathrin-mediated endocytosis of synaptic vesicle membranes involves the recruitment of clathrin and AP-2 adaptor complexes to the presynaptic plasma membrane. Phosphoinositides have been implicated in nucleating coat assembly by directly binding to several endocytotic proteins including AP-2 and AP180. Here, we show that the stimulatory effect of ATP and GTP{gamma}S on clathrin coat recruitment is mediated at least in part by increased levels of PIP2. We also provide evidence for a role of ADP-ribosylation factor 6 (ARF6) via direct stimulation of a synaptically enriched phosphatidylinositol 4-phosphate 5-kinase type I{gamma} (PIPKI{gamma}), in this effect. These data suggest a model according to which activation of PIPKI{gamma} by ARF6-GTP facilitates clathrin-coated pit assembly at the synapse.

Key Words: ARF; clathrin coat assembly; PIPK I{gamma}; PIP2 formation; endocytosis

M. Kinuta and M.R. Wenk contributed equally to this paper.

* Abbreviations used in this paper: ARF, ADP-ribosylation factor; DTSP, 3,3'-Dithio-bis(propionic acid N-hydroxysuccinimide ester); GEF, guanine nucleotide exchange factor; LP2, lysed synaptosomal membrane fraction; PH, pleckstrin homology; PI(4,5)P2, phosphatidylinositol (4,5)-bisphosphate; PIPKI{gamma}, phosphatidylinositol 4-phosphate 5-kinase type I{gamma}; PLD, phospholipase D; SV, synaptic vesicles.


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