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J. Biol. Chem., Vol. 281, Issue 29, 20542-20554, July 21, 2006

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Differential Actin-dependent Localization Modulates the Evolutionarily Conserved Activity of Shroom Family Proteins^*

Megan L. Dietz, Teresa M. Bernaciak, Frank Vendetti, Joseph M. Kielec, and Jeffrey D. Hildebrand¹

From the Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260

Shroom is an actin-associated determinant of cell morphology that is required for neural tube closure in both mice and frogs. Shroom regulates this process by causing apical constriction of epithelial cells via a pathway involving myosin II. Here we report on characterization of the Shroom-related proteins Apxl and KIAA1202 and their role in cell architecture. Shroom, Apxl, and KIAA1202 exhibit differing abilities to interact with the actin cytoskeleton. In fibroblasts, Shroom readily associates with actin stress fibers and induces bundling, Apxl is found on cortical actin, and KIAA1202 is localized to a cytoplasmic population of F-actin. In epithelial cells, Apxl and KIAA1202 do not induce apical constriction as Shroom does, but have the capacity to do so if targeted to the apical junctional complex. To determine whether the activity of Shroom-like proteins is conserved in invertebrates, we have tested the ability of the lone Shroomrelated protein in Drosophila, CG8603, to activate the constriction pathway. A chimeric protein consisting of the Shroom targeting domain and the Drosophila protein elicits constriction. Finally, we show that Apxl is involved in regulating the cytoskeletal organization and architecture of endothelial cells. We predict that the ability of Shroom-like proteins to regulate cellular morphology is conserved in evolution and is regulated in part by subcellular localization.

Received for publication, November 21, 2005 , and in revised form, March 22, 2006.

This article is dedicated to the memory of our friend and colleague Megan L. Dietz who died suddenly and unexpectedly during the course of this work.

^* This work was supported by NIGMS, National Institutes of Health, Grant RO1GM067525 (to J. D. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. S1.

Deceased.

¹ To whom correspondence should be addressed: 4249 Fifth Ave., Pittsburgh, PA 15260. Tel.: 412-624-6987; Fax: 412-624-4759; E-mail: jeffh{at}pitt.edu.

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