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Establishment of the Circumferential Actin Filament Network Is a Prerequisite for Localization of the Cadherin-Catenin Complex in Epithelial Cells¹

Department of Microbiology and Immunology, University of Tennessee, Memphis, Tennessee 38163

With the adhesion molecules, the actin cytoskeleton controls cell-cell and cell-substrate interactions and participates in transmembrane signaling. The relationships between actin and adhesion complexes at the sites of adhesion have been well documented. Here we investigate by a series of studies whether a relationship exists between actin organization and the localization and function of the components of the cadherin-catenin complex (CCC) that participates in the cell-cell adherens junction. Reversible actin depolymerization reversibly affects the peripheral distribution of CCCs. Mutations in adenovirus E1A and the small GTPase rac1, but not Ha-ras, disrupt the circumferential, cortical actin filament (CAF) network and the targeting of CCC components to the cell surface. Disruption of actin stress fibers or microtubules does not interfere with CCC localization and function. Constitutive loss of the apical cortical actin ring results in epithelial cells in which components of the CCCs are found only in intracellular vesicles and never at the surface. A kinetic analysis of the de novo appearance of the CAF network and the CCCs at the cell surface was also conducted. When F-actin was dissolved, surface CCC components were internalized. Reestablishment of CAFs required about 4 h, during which time E-cadherin and -catenin were found first in a juxtanuclear location and then in intracellular vesicles or post-Golgi carriers, similar to what was observed in cells expressing mutant E1A or rac1. Thus, disruption of preexisting CCCs resulted in their internalization and recycling to the Golgi. It was only after the regeneration of the filamentous actin ring beneath the cell surface that peripheral localization of CCCs was observed. A similar result was observed with dominant negative rac1. These data suggest that the status of cortical actin is assessed and transduced and thereby regulates the transport and delivery of cadherin and catenins to the cell surface.

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