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J Biol Chem, Vol. 274, Issue 19, 12990-12995, May 7, 1999
From the Departments of Pharmacology and Cancer Biology and of
Biochemistry, Duke University Medical Center,
Durham, North Carolina 27710
The SAC1 gene product has been
implicated in the regulation of actin cytoskeleton, secretion from the
Golgi, and microsomal ATP transport; yet its function is unknown.
Within SAC1 is an evolutionarily conserved 300-amino acid
region, designated a SAC1-like domain, that is also present
at the amino termini of the inositol polyphosphate 5-phosphatases,
mammalian synaptojanin, and certain yeast INP5 gene
products. Here we report that SAC1-like domains have
intrinsic enzymatic activity that defines a new class of polyphosphoinositide phosphatase (PPIPase). Purified recombinant SAC1-like domains convert yeast lipids phosphatidylinositol
(PI) 3-phosphate, PI 4-phosphate, and PI 3,5-bisphosphate to PI,
whereas PI 4,5-bisphosphate is not a substrate. Yeast lacking Sac1p
exhibit 10-, 2.5-, and 2-fold increases in the cellular levels of PI
4-phosphate, PI 3,5-bisphosphate, and PI 3-phosphate, respectively. The
5-phosphatase domains of synaptojanin, Inp52p, and Inp53p are also
catalytic, thus representing the first examples of an inositol
signaling protein with two distinct lipid phosphatase active sites
within a single polypeptide chain. Together, our data provide a long sought mechanism as to how defects in Sac1p overcome certain actin mutants and bypass the requirement for yeast
phosphatidylinositol/phosphatidylcholine transfer protein, Sec14p. We
demonstrate that PPIPase activity is a key regulator of membrane
trafficking and actin cytoskeleton organization and suggest signaling
roles for phosphoinositides other than PI 4,5-bisphosphate in these
processes. Additionally, the tethering of PPIPase and 5-phosphatase
activities indicate a novel mechanism by which concerted
phosphoinositide hydrolysis participates in membrane trafficking.
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