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J. Biol. Chem., Vol. 279, Issue 36, 38025-38031, September 3, 2004

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Myosin VI Regulates Endocytosis of the Cystic Fibrosis Transmembrane Conductance Regulator^*

Agnieszka Swiatecka-Urban, Cary Boyd, Bonita Coutermarsh, Katherine H. Karlson, Roxanna Barnaby, Laura Aschenbrenner¶, George M. Langford||, Tama Hasson¶, and Bruce A. Stanton

From the Dartmouth Medical School, Department of Physiology, Hanover, New Hampshire 03755, the ^¶University of California at San Diego, Section of Cell and Developmental Biology, La Jolla, California 92093, and ^||Dartmouth College, Department of Biological Sciences, Hanover, New Hampshire 03755

The cystic fibrosis transmembrane conductance regulator (CFTR) is a cyclic AMP-regulated Cl^- channel expressed in the apical plasma membrane in fluid-transporting epithelia. Although CFTR is rapidly endocytosed from the apical membrane of polarized epithelial cells and efficiently recycled back to the plasma membrane, little is known about the molecular mechanisms regulating CFTR endocytosis and endocytic recycling. Myosin VI, an actin-dependent, minus-end directed mechanoenzyme, has been implicated in clathrin-mediated endocytosis in epithelial cells. The goal of this study was to determine whether myosin VI regulates CFTR endocytosis. Endogenous, apical membrane CFTR in polarized human airway epithelial cells (Calu-3) formed a complex with myosin VI, the myosin VI adaptor protein Disabled 2 (Dab2), and clathrin. The tail domain of myosin VI, a dominant-negative recombinant fragment, displaced endogenous myosin VI from interacting with Dab2 and CFTR and increased the expression of CFTR in the plasma membrane by reducing CFTR endocytosis. However, the myosin VI tail fragment had no effect on the recycling of endocytosed CFTR or on fluid-phase endocytosis. CFTR endocytosis was decreased by cytochalasin D, an actin-filament depolymerizing agent. Taken together, these data indicate that myosin VI and Dab2 facilitate CFTR endocytosis by a mechanism that requires actin filaments.

Received for publication, March 22, 2004 , and in revised form, June 16, 2004.

^* This study was supported by National Institutes of Health Grant 1 P20-RR018787-01 (to A. S.-U.), Grant RO1-EY12695 (to T. H.), Grant RO1-DK45881 (to B. A. S.), Grant RO1-DK34533 (to B. A. S.), and Grant 1 P20-RR018787-01 (to B. A. S.); a Shwachman Award (to A. S.-U.) and a Research Development Program Grant (to B. A. S.) from the Cystic Fibrosis Foundation; and March of Dimes Birth Defects Foundation Grant 6-FY02-150 (to T. H.). 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: Dept. of Physiology, Dartmouth Medical School, Hanover, NH 03755. Tel.: 603-650-1534; Fax: 603-650-1130; E-mail: Agnieszka.Swiatecka-Urban{at}Dartmouth.edu.

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