Abstract

Apical constriction is a widely utilized cell shape change linked to folding, bending and invagination of polarized epithelia. It remains unclear how apical constriction is regulated spatiotemporally during tissue invagination and how this cellular process contributes to tube formation in different developmental contexts. Using Drosophila salivary gland (SG) invagination as a model, we show that regulation of folded gastrulation expression by the Fork head transcription factor is required for apicomedial accumulation of Rho kinase and non-muscle myosin II, which coordinate apical constriction. We demonstrate that neither loss of spatially coordinated apical constriction nor its complete blockage prevent internalization and tube formation, although such manipulations affect the geometry of invagination. When apical constriction is disrupted, compressing force generated by a tissue-level myosin cable contributes to SG invagination. We demonstrate that fully elongated polarized SGs can form outside the embryo, suggesting that tube formation and elongation are intrinsic properties of the SG.

Highlights

  • Organs that transport gases and nutrients, as well as those producing and secreting vital hormones and enzymes, are organized as epithelial tubes, many of which arise from already polarized epithelial sheets (Andrew and Ewald, 2010)

  • At early stage 11, all salivary gland (SG) cells were on the embryo surface and cells with different apical area were distributed relatively randomly, cells with small and large apical area tended to be toward the inside and at the periphery of the tissue, respectively (Before invagination; Figure 1D and D’)

  • Apical constriction often occurs as polarized epithelial precursors bend, fold and invaginate to form different tissues and organs (Martin and Goldstein, 2014)

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Summary

Introduction

Organs that transport gases and nutrients, as well as those producing and secreting vital hormones and enzymes, are organized as epithelial tubes, many of which arise from already polarized epithelial sheets (Andrew and Ewald, 2010). A subset of cells extend out of the plane of the epithelium in an orthogonal direction to form a tube; this process is observed during branching morphogenesis of many organs, including the mammalian lungs and kidney, and the primary branches of the Drosophila trachea (Andrew and Ewald, 2010; Lubarsky and Krasnow, 2003). A limited number of cellular processes are involved in creating three-dimensional structures, which include regulated changes in cell shape, arrangement and position, as well as oriented cell divisions and spatially restricted programmed cell death (Andrew and Ewald, 2010). In polarized epithelial cells that maintain cell-cell adhesion, apical constriction is linked to tissue folding or invagination (Alvarez and Navascues, 1990; Hardin and Keller, 1988; Kam et al, 1991; Lewis, 1947; Sweeton et al, 1991; Wallingford et al, 2013)

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