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Originally published as MBC in Press, 10.1091/mbc.E03-05-0297 on October 3, 2003

Vol. 15, Issue 1, 24-36, January 2004

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Vacuole Size Control: Regulation of PtdIns(3,5)P2 Levels by the Vacuole-associated Vac14-Fig4 Complex, a PtdIns(3,5)P2-specific Phosphatase

Simon A. Rudge, Deborah M. Anderson, and Scott D. Emr *

Department of Cellular and Molecular Medicine, and the Howard Hughes Medical Institute, University of California at San Diego, School of Medicine, La Jolla, California 92093-0668

Submitted May 13, 2003; Revised August 8, 2003; Accepted August 28, 2003
Monitoring Editor: Benjamin Glick

In the budding yeast Saccharomyces cerevisiae, phosphatidylinositol 3,5-bisphosphate (PtdIns(3,5)P2) is synthesized by a single phosphatidylinositol 3-phosphate 5-kinase, Fab1. Cells deficient in PtdIns(3,5)P2 synthesis exhibit a grossly enlarged vacuole morphology, whereas increased levels of PtdIns(3,5)P2 provokes the formation of multiple small vacuoles, suggesting a specific role for PtdIns(3,5)P2 in vacuole size control. Genetic studies have indicated that Fab1 kinase is positively regulated by Vac7 and Vac14; deletion of either gene results in ablation of PtdIns(3,5)P2 synthesis and the formation of a grossly enlarged vacuole. More recently, a suppressor of vac7{Delta} mutants was identified and shown to encode a putative phosphoinositide phosphatase, Fig4. We demonstrate that Fig4 is a magnesium-activated PtdIns(3,5)P2-selective phosphoinositide phosphatase in vitro. Analysis of a Fig4-GFP fusion protein revealed that the Fig4 phosphatase is localized to the limiting membrane of the vacuole. Surprisingly, in the absence of Vac14, Fig4-GFP no longer localizes to the vacuole. However, Fig4-GFP remains localized to the grossly enlarged vacuoles of vac7 deletion mutants. Consistent with these observations, we found that Fig4 physically associates with Vac14 in a common membrane–associated complex. Our studies indicate that Vac14 both positively regulates Fab1 kinase activity and directs the localization/activation of the Fig4 PtdIns(3,5)P2 phosphatase.

Article published online ahead of print. Mol. Biol. Cell 10.1091/mbc.E03–05–0297. Article and publication date are available at www.molbiolcell.org/cgi/doi/10.1091/mbc.E03-05-0297.

* Corresponding author. E-mail address: semr{at}ucsd.edu.




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