Organ positioning in Drosophila requires complex tissue–tissue interactions

Abstract

Positioning an organ with respect to other tissues is a complex process necessary for proper anatomical development and organ function. The local environment surrounding an organ can serve both as a substrate for migration and as a source of guidance cues that direct migration. Little is known about the factors guiding Drosophila salivary gland movement or about the contacts the glands establish along their migratory path. Here, we provide a detailed description of the spatial and temporal interactions between the salivary glands and surrounding tissues during embryogenesis. The glands directly contact five other tissues: the visceral mesoderm, gastric caecae, somatic mesoderm, fat body, and central nervous system. Mutational analysis reveals that all of the tissues tested in this study are important for normal salivary gland positioning; proper differentiation of the visceral and somatic mesoderm is necessary for the glands to attain their final correct position. We also provide evidence that the segment-polarity gene, gooseberry (gsb), controls expression of signals from the developing fat body that direct posterior migration of the glands. These data further the understanding of how organ morphology and position are determined by three-dimensional constraints and guidance cues provided by neighboring tissues.

Rho GTPase controls Drosophila salivary gland lumen size through regulation of the actin cytoskeleton and Moesin

“…After invaginating from the ventral surface of the embryo, salivary gland cells migrate collectively as an intact tube, with the distal tip cells elongating and extending protrusions in the direction of migration (Bradley et al, 2003), and the proximal end cells changing shape from columnar to cuboidal (Xu et al, 2008). When the distal gland cells contact the overlying circular visceral mesoderm (CVM), the entire gland turns and migrates posteriorly (Bradley et al, 2003;Vining et al, 2005). Contact between the distal gland cells and the CVM is mediated through the integrin adhesion receptors; loss of the PS or the PS2 integrin subunits results in glands that fail to turn and migrate posteriorly (Bradley et al, 2003).…”

The Garz Sec7 domain guanine nucleotide exchange factor for Arf regulates salivary gland development in Drosophila

“…Flies with defects in genes encoding various adhesion molecules, such as integrins or DE-cadherin exhibit defects in tube elongation and abnormal cellular shape. [15][16][17][18][19][20][21] Defects in adhesion result in small, poorly organized salivary glands. 22 We posited that similar phenotypes might be apparent if Garz pathway, inhibits trafficking of adhesion molecules DE-cadherin (DE-cad) and Flamingo to the cell surface, disrupts the localization of the tumor suppressor Discs large (Dlg) involved in polarity determination and causes a dramatic disorganization of the salivary gland.…”

Different Wnt signals act through the Frizzled and RYK receptors duringDrosophilasalivary gland migration

“…During this phase of migration, the salivary gland tip cells extend lamellipodial protrusions and, using integrin-based motility, actively travel along the visceral mesoderm. The substrate for this movement is the circular visceral mesoderm (CVM) that will ultimately form the inner layer of the gut muscle (Bradley et al, 2003;Kerman et al, 2006;Vining et al, 2005). During their migration, the glands are guided by the chemoattractant Netrin and the chemorepellent Slit to arrive at their correct position within the embryo (Kolesnikov and Beckendorf, 2005).…”