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J. Biol. Chem., Vol. 282, Issue 32, 23725-23736, August 10, 2007

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Myosin Vb Is Required for Trafficking of the Cystic Fibrosis Transmembrane Conductance Regulator in Rab11a-specific Apical Recycling Endosomes in Polarized Human Airway Epithelial Cells^*

Agnieszka Swiatecka-Urban¹, Laleh Talebian, Eiko Kanno, Sophie Moreau-Marquis, Bonita Coutermarsh, Karyn Hansen, Katherine H. Karlson, Roxanna Barnaby, Richard E. Cheney^¶, George M. Langford^||, Mitsunori Fukuda^**, and Bruce A. Stanton

From the Department of Physiology, Dartmouth Medical School, and the ^||Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755, the Fukuda Initiative Research Unit, Institute of Physical and Chemical Research (RIKEN), 2-1 Hirosawa, Wako, Saitama 351-0198, Japan, the ^¶Department of Cell and Molecular Physiology, University of North Carolina, Chapel Hill, North Carolina 27599, and the ^**Department of Developmental Biology and Neurosciences, Laboratory of Membrane Trafficking Mechanisms, Graduate School of Life Sciences, Tohoku University, Aobayama, Aoba-ku, Sendai, Miyagi 980-8578, Japan

Cystic fibrosis transmembrane conductance regulator (CFTR)-mediated Cl^- secretion across fluid-transporting epithelia is regulated, in part, by modulating the number of CFTR Cl^- channels in the plasma membrane by adjusting CFTR endocytosis and recycling. However, the mechanisms that regulate CFTR recycling in airway epithelial cells remain unknown, at least in part, because the recycling itineraries of CFTR in these cells are incompletely understood. In a previous study, we demonstrated that CFTR undergoes trafficking in Rab11a-specific apical recycling endosomes in human airway epithelial cells. Myosin Vb is a plus-end-directed, actin-based mechanoenzyme that facilitates protein trafficking in Rab11a-specific recycling vesicles in several cell model systems. There are no published studies examining the role of myosin Vb in airway epithelial cells. Thus, the goal of this study was to determine whether myosin Vb facilitates CFTR recycling in polarized human airway epithelial cells. Endogenous CFTR formed a complex with endogenous myosin Vb and Rab11a. Silencing myosin Vb by RNA-mediated interference decreased the expression of wild-type CFTR and F508-CFTR in the apical membrane and decreased CFTR-mediated Cl^- secretion across polarized human airway epithelial cells. A recombinant tail domain fragment of myosin Vb attenuated the plasma membrane expression of CFTR by arresting CFTR recycling. The dominant-negative effect was dependent on the ability of the myosin Vb tail fragment to interact with Rab11a. Taken together, these data indicate that myosin Vb is required for CFTR recycling in Rab11a-specific apical recycling endosomes in polarized human airway epithelial cells.

Received for publication, September 5, 2006 , and in revised form, April 2, 2007.

^* This work was supported by National Institutes of Health Grant P20-RR018787 (to A. S.-U.), Grant RO1-DC03299 (to R. E. C.), and Grants RO1-DK45881, RO1-DK34533, and P20-RR018787 (to B. A. S.) from the National Center for Research Resources and by Shwachman Award SWIATE03QO (to A. S.-U.) and a research development program grant (to B. A. S.) from the Cystic Fibrosis Foundation. 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.

¹ To whom correspondence should be addressed. E-mail: asurban{at}pitt.edu.

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