Early Genes Required for Salivary Gland Fate Determination and Morphogenesis in Drosophila melanogaster

Abstract

Studies of Drosophila salivary gland formation have elucidated the regulatory pathway by which the salivary gland fate is determined and the morphogenetic processes by which the primordial cells are internalized to form the tubular glands. Both the position of the salivary primordia and the number of cells recruited to a salivary gland fate are established through a combination of the localized expression of the transcription factors SEX COMBS REDUCED (SCR), TEASHIRT (TSH) and ABDOMINAL-B (ABD-B), and localized DPP-signaling. Similarly, the distinction between the two major cell types, duct and secretory, is determined by spatially limited EGF-signaling. Salivary gland formation also requires the function of two transcription factors expressed in nearly all cells of the developing embryo, EXTRADENTICLE (EXD) and HOMOTHORAX (HTH). Once the salivary gland fate is determined, cells of the secretory primordia are internalized by an apical constriction mode of invagination. We have characterized three genes encoding transcription factors, trachealess (trh), hückebein (hkb), and fork head (fkh), that are downstream targets of the salivary gland regulators. Mutations in these transcription factors profoundly affect salivary gland morphogenesis. trh is required for the formation of the salivary duct tubes. hkb determines the order of secretory cell invagination, a regulated process critical for determining the final shape of the salivary gland. fkh has two early roles in salivary gland formation. fkh both promotes secretory cell survival and facilitates secretory cell internalization. trh, hkb, and fkh are involved in the formation of not only the salivary duct and secretory tubes, but also of other tubular structures, such as the trachea and the gut endoderm. We propose that trh, hkb, and fkh may serve as "morphogenetic cassettes" responsible for forming tubular structures in a variety of tissues.

Interface Contractility between Differently Fated Cells Drives Cell Elimination and Cyst Formation

“…To test whether fate misspecification in Psc/Su(z)2 clones underlied cyst formation, we individually overexpressed unrelated transcription factors silenced by Psc/Su(z)2 ( Figure S1 M) using the GAL4/UAS flip-out system [ 30 ]. Intriguingly, ectopic expression of the forkhead-box transcription factor fork head ( fkh ) involved in salivary gland morphogenesis ( Figures 1 G–1I and S2 A–S2D) [ 31 ], the homeobox factor Abdominal-B ( AbdB ) involved in segment specification ( Figure S2 F) [ 32 ], or the Runt-domain factor lozenge ( lz ) required for hemocyte differentiation (see Figure S2 F) [ 33 ] were each sufficient to give rise to cysts. This suggests that ectopic activation of Polycomb-silenced cell-fate-specifying transcription factors may be sufficient to drive cyst formation in Psc/Su(z)2 clones.…”

The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity

“…The SG comprises two large secretory tubes, each containing 100 polarized epithelial cells that are specialized for the production and delivery of secreted proteins. Consistent with the high-level secretory activity of the SG, at least 34 secretory pathway component genes (SPCGs) are highly expressed in the secretory cells (Abrams and Andrew, 2005), and this expression requires at least two transcription factor genes, fork head (fkh) and CrebA (Andrew et al, 1997;Myat et al, 2000).…”

Tissue remodeling: a mating-induced differentiation program for the Drosophilaoviduct

“…Studies of these organs reveal a general program for tubular organ development, in which combinatorial expression of global patterning genes specifies positions within the embryo for the subsequent activation of tissue-specific early genes and transcription factors. This program results in the activation of downstream genes involved in terminal differentiation of organ-specific specializations such as the cuticle that lines the tracheal lumen [ 1 , 2 , 4 , 7 - 9 ].…”