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Vol. 15, Issue 7, 3196-3209, July 2004

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Soi3p/Rav1p Functions at the Early Endosome to Regulate Endocytic Trafficking to the Vacuole and Localization of Trans-Golgi Network Transmembrane Proteins

György Sipos ^*  , Jason H. Brickner ^*  , E.J. Brace ^*, Linyi Chen ^|| ¶, Alain Rambourg ^#, Francois Kepes ^# @, and Robert S. Fuller ^* **

^* Department of Biological Chemistry, University of Michigan Medical Center, Ann Arbor, Michigan 48109-0606; ^|| Department of Pharmacology, Wayne State University School of Medicine, Detroit, Michigan 48201, France; and ^# Departement de Biologie Cellulaire et Moleculaire, Commissariat á l'Energie Atomique Saclay, Gif-sur-Yvette 91191 Cedex, France

Submitted October 22, 2003; Revised April 5, 2004; Accepted April 7, 2004
Monitoring Editor: Randy Schekman

SOI3 was identified by a mutation, soi3-1, that suppressed a mutant trans-Golgi network (TGN) localization signal in the Kex2p cytosolic tail. SOI3, identical to RAV1, encodes a protein important for regulated assembly of vacuolar ATPase. Here, we show that Soi3/Rav1p is required for transport between the early endosome and the late endosome/prevacuolar compartment (PVC). By electron microscopy, soi3-1 mutants massively accumulated structures that resembled early endosomes. soi3 mutants exhibited a kinetic delay in transfer of the endocytic tracer dye FM4-64, from the 14°C endocytic intermediate to the vacuole. The soi3 mutation delayed vacuolar degradation but not internalization of the a-factor receptor Ste3p. By density gradient fractionation, Soi3/Rav1p associated as a peripheral protein with membranes of a density characteristic of early endosomes. The soi3 null mutation markedly reduced the rate of Kex2p transport from the TGN to the PVC but had no effect on vacuolar protein sorting or cycling of Vps10p. These results suggest that assembly of vacuolar ATPase at the early endosome is required for transport of both Ste3p and Kex2p from the early endosome to the PVC and support a model in which cycling through the early endosome is part of the normal itinerary of Kex2p and other TGN-resident proteins.

Abbreviations used: ALP, alkaline phosphatase; API, aminopeptidase I; C-tail, cytosolic tail; GFP, green fluorescent protein; HA, hemagglutinin epitope; IP, immunoprecipitation; PVC, prevacuolar compartment; TLS, trans-Golgi network localization signal; Vps, vacuolar protein sorting.

These authors made comparable contributions to this work.

Present address: Department of Medical Biochemistry, University and Biocenter of Vienna, A-1030 Vienna, Austria

Present address: Department of Biochemistry and Biophysics, University of California, San Francisco, CA 94143

^¶ Present address: Department of Molecular and Integrative Physiology, University of Michigan Medical Center, Ann Arbor, MI 48109-0622

^@ Present address: Dynamique de la Compartimentation Cellulaire, Institut des Sciences du Végétal, Centre National de la Recherche Scientifique Unité Propre de Recherche 2355, Gif-sur-Yvette, France, and Epigenomics Project/Genopole, Evry, France

^** Corresponding author. E-mail address: bfuller{at}umich.edu.

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