Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1

Thomas J Widmann,Christian Dahmann

doi:10.1242/jcs.044271

Abstract

Morphogenesis is largely driven by changes in the shape of individual cells. However, how cell shape is regulated in developing animals is not well understood. Here, we show that the onset of TGFbeta/Dpp signaling activity correlates with the transition from cuboidal to columnar cell shape in developing Drosophila melanogaster wing disc epithelia. Dpp signaling is necessary for maintaining this elongated columnar cell shape and overactivation of the Dpp signaling pathway results in precocious cell elongation. Moreover, we provide evidence that Dpp signaling controls the subcellular distribution of the activities of the small GTPase Rho1 and the regulatory light chain of non-muscle myosin II (MRLC). Alteration of Rho1 or MRLC activity has a profound effect on apical-basal cell length. Finally, we demonstrate that a decrease in Rho1 or MRLC activity rescues the shortening of cells with compromised Dpp signaling. Our results identify a cell-autonomous role for Dpp signaling in promoting and maintaining the elongated columnar shape of wing disc cells and suggest that Dpp signaling acts by regulating Rho1 and MRLC.

Highlights

Cell growth, cell fate specification and morphogenesis are processes important for animal development
We show that the onset of Transforming growth factor β (TGFβ)/Dpp signaling activity correlates with the transition from cuboidal to columnar cell shape in developing Drosophila melanogaster wing disc epithelia
We provide evidence that Dpp signaling controls the subcellular distribution of the activities of the small GTPase Rho1 and the regulatory light chain of non-muscle myosin II (MRLC)

Summary

Introduction

Cell fate specification and morphogenesis are processes important for animal development. Less is known about how morphogenesis is regulated and how cell fate specification, growth and morphogenesis are orchestrated during animal development. One important class of regulators of actin-dependent change in cell shape is the Rho family of small GTPases (reviewed by Jaffe and Hall, 2005; Van Aelst and Symons, 2002). Rho signaling and myosin II are required for a variety of developmental processes, including apical constriction of epithelial cells during vertebrate neural tube formation, tubular morphogenesis, morphogenetic furrow progression and ventral furrow formation in Drosophila (Brodu and Casanova, 2006; Corrigall et al, 2007; Dawes-Hoang et al, 2005; Escudero et al., 2007; Fox and Peifer, 2007; Kolsch et al, 2007; Nikolaidou and Barrett, 2004; Simoes et al, 2006; Wei et al, 2001), as well as cell rearrangements in the plane of the epithelium (Bertet et al, 2004; Escudero et al, 2007)

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