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J. Biol. Chem., Vol. 279, Issue 19, 20392-20400, May 7, 2004

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Role of Src-induced Dynamin-2 Phosphorylation in Caveolae-mediated Endocytosis in Endothelial Cells^*

Ayesha N. Shajahan, Barbara K. Timblin, Raudel Sandoval, Chinnaswamy Tiruppathi, Asrar B. Malik, and Richard D. Minshall¶

From the Departments of Pharmacology and Anesthesiology, University of Illinois, College of Medicine, Chicago, Illinois 60612

Albumin transcytosis, a determinant of transendothelial permeability, is mediated by the release of caveolae from the plasma membrane. We addressed the role of Src phosphorylation of the GTPase dynamin-2 in the mechanism of caveolae release and albumin transport. Studies were made in microvascular endothelial cells in which the uptake of cholera toxin subunit B, a marker of caveolae, and ¹²⁵I-albumin was used to assess caveolae-mediated endocytosis. Albumin binding to the 60-kDa cell surface albumin-binding protein, gp60, induced Src activation (phosphorylation on Tyr⁴¹⁶) within 1 min and resulted in Src-dependent tyrosine phosphorylation of dynamin-2, which increased its association with caveolin-1, the caveolae scaffold protein. Expression of kinase-defective Src mutant interfered with the association between dynamin-2, which caveolin-1 and prevented the uptake of albumin. Expression of non-Src-phosphorylatable dynamin (Y231F/Y597F) resulted in reduced association with caveolin-1, and in contrast to WT-dynamin-2, the mutant failed to translocate to the caveolin-rich membrane fraction. The Y231F/Y597F dynamin-2 mutant expression also resulted in impaired albumin and cholera toxin subunit B uptake and reduced transendothelial albumin transport. Thus, Src-mediated phosphorylation of dynamin-2 is an essential requirement for scission of caveolae and the resultant transendothelial transport of albumin.

Received for publication, August 6, 2003 , and in revised form, March 5, 2004.

^* This work was supported in part by National Institutes of Health Grants T32 HL07239, HL60678 (to A. B. M.), GM58531 (to C. T.), and HL71626 (to R. D. M.). 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.

^¶ A Parker B. Francis Fellow in Pulmonary Research. To whom correspondence should be addressed: Dept. of Pharmacology, University of Illinois, M/C 868, 835 S. Wolcott Ave., Chicago, IL 60612. Tel.: 312-996-1655; Fax: 312-996-1225; E-mail: rminsh{at}uic.edu.

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