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J. Biol. Chem., Vol. 279, Issue 29, 30622-30633, July 16, 2004

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Phosphatidylinositol 4,5-Bisphosphate Regulates Adipocyte Actin Dynamics and GLUT4 Vesicle Recycling^*

Makoto Kanzaki, Megumi Furukawa, William Raab, and Jeffrey E. Pessin

From the Department of Pharmacological Sciences, State University of New York at Stony Brook, Stony Brook, New York 11794

To investigate the potential role of phosphatidylinositol 4, 5-bisphosphate (PI(4,5)P₂) in the regulation of actin polymerization and GLUT4 translocation, the type I phosphatidylinositol 4-phosphate 5-kinases (PIP5Ks) were expressed in 3T3L1 adipocytes. In preadipocytes (fibroblasts) PIP5K expression promoted actin polymerization on membrane-bound vesicles to form motile actin comets. In contrast, expression of PIP5K in differentiated 3T3L1 adipocytes resulted in the formation of enlarged vacuole-like structures coated with F-actin, cortactin, dynamin, and N-WASP. Treatment with either latrunculin B (an inhibitor for actin polymerization) or Clostridium difficile toxin B (a general Rho family inhibitor) resulted in a relatively slower disappearance of coated F-actin from these vacuoles, but the vacuoles themselves remained unaffected. Functionally, the increased PI(4,5)P₂ levels resulted in an inhibition of transferrin receptor and GLUT4 endocytosis and a slow accumulation of these proteins in the PI(4,5)P₂-enriched vacuoles along with the non-clathrin-derived endosome marker (caveolin) and the AP-2 adaptor complex. However, these structures were devoid of early endosome markers (EEA1, clathrin) and the biosynthetic membrane secretory machinery markers p115 (Golgi) and syntaxin 6 (trans-Golgi Network). Taken together, these data demonstrate that PI(4,5)P₂ has distinct morphologic and functional properties depending upon specific cell context. In adipocytes, altered PI(4,5)P₂ metabolism has marked effects on GLUT4 endocytosis and intracellular vesicle trafficking due to the derangement of actin dynamics.

Received for publication, February 9, 2004 , and in revised form, April 26, 2004.

^* This work was supported by Research Grants DK33823 and DK59291 from the National Institutes of Health (to J. E. P.) and Grant 1-03-JF-14 from the American Diabetes Association (to M. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Tohoku University Biomedical Engineering Research Organization (TUBERO), Bldg. 1, Graduate School of Medicine, 2-1 Seiryo-machi, Aoba, Sendai, Miyag 980-8575, Japan. Tel.: 81-22-717-7581; Fax: 81-22-717-7873; E-mail: kanzaki{at}tubero.tohoku.ac.jp.

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