Border of Notch activity establishes a boundary between the two dorsal appendage tube cell types

Abstract

Boundaries establish and maintain separate populations of cells critical for organ formation. We show that Notch signaling establishes the boundary between two types of post-mitotic epithelial cells, the Rhomboid- and the Broad-positive cells. These cells will undergo morphogenetic movements to generate the two sides of a simple organ, the dorsal appendage tube of the Drosophila egg chamber. The boundary forms due to a difference in Notch levels in adjacent cells. The Notch expression pattern mimics the boundary; Notch levels are high in Rhomboid cells and low in Broad cells. Notch(-) mutant clones generate an ectopic boundary: ectopic Rhomboid cells arise in Notch(+) cells adjacent to the Notch(-) mutant cells but not further away from the clonal border. Pangolin, a component of the Wingless pathway, is required for Broad expression and for rhomboid repression. We further show that Broad represses rhomboid cell autonomously. Our data provide a foundation for understanding how a single row of Rhomboid cells arises adjacent to the Broad cells in the dorsal appendage primordia. Generating a boundary by the Notch pathway might constitute an evolutionarily conserved first step during organ formation in many tissues.

Conditional Switches for Extracellular Matrix Patterning inDrosophila melanogaster

“…Finally, pointed encodes an ETS-domain transcription factor activated by EGFR signaling (summarized in Figure 1). The data are consistent with a model in which Notch signaling and EGFR signaling through Pointed cooperate to specify the midline branch that results in two distinct DAs (Ward et al 2006).…”

“…At least two distinct groups of the columnar follicle cells then reorganize to create the DAs; ''roof'' cells express the transcription factor Broad and constrict their cytoskeleton on the apical side, while ''floor'' cells express Rhomboid (Dorman et al 2004). Notch signaling acts to create the boundary between the roof and floor cell types (Ward et al 2006). The coordinated anterior migration of the roof and floor cells extends the DAs and this involves additional signaling through the Jun-kinase ( JNK) pathway.…”

Feedback control of the EGFR signaling gradient: superposition of domain-splitting events inDrosophilaoogenesis

“…The resulting gradient of EGFR activation controls a number of transcription factors, signaling molecules and effector genes required for eggshell morphogenesis (Cavaliere et al, 2008;Dobens and Raftery, 2000;Wu et al, 2008;Yakoby et al, 2008a). Several other pathways, including Decapentaplegic (DPP) and Notch, are also involved in this process (Deng and Bownes, 1997;Twombly et al, 1996;Ward et al, 2006), but their role is secondary to that of the EGFR pathway as the dorsal eggshell structures are completely abolished in the absence of GRK (Schupbach, 1987).…”

Gene regulation during Drosophila eggshell patterning

“…As mentioned in the previous section, one of the main regulators of rho is BR, which represses rho in cells that form the upper part of the future dorsal appendages (11,43). At this point of oogenesis, br is regulated by the brL enhancer.…”

“…Indeed, the wild-type expression of rho in both species can be predicted by the expression pattern of br. In both species, rho is expressed at the anterior border of the br domain (11,21,30,43). If this is correct, then the regulatory region of brL should be changed in a way that alters the lateral extent of its activity.…”