Expression patterns of cadherin genes in Drosophila oogenesis

Abstract

In Drosophila oogenesis, the follicular epithelium that envelops the oocyte is patterned by a small set of inductive signals and gives rise to an elaborate three-dimensional eggshell. Several eggshell structures provide sensitive readouts of the patterning signals, but the formation of these structures is still poorly understood. In other systems, epithelial morphogenesis is guided by the spatial patterning of cell adhesion and cytoskeleton genes. As a step towards developing a comprehensive description of patterning events leading to eggshell morphogenesis, we report the expression of Drosophila cadherins, calcium dependent adhesion molecules that are repeatedly used throughout development. We found that 9/17 of Drosophila cadherins are expressed in the follicular epithelium in dynamic patterns during oogenesis. In late oogenesis, the expression patterns of cadherin genes in the main body follicle cells is summarized using a compact set of simple geometric shapes, reflecting the integration of the EGFR and DPP inductive signals. The multi-layered composite patterning of the cadherins is hypothesized to play a key role in the formation of the eggshell. Of particular note is the complex patterning of the region of the follicular epithelium that gives rise to the dorsal appendages, which are tubular structures that serve as respiratory organs for the developing embryo.

Three-Dimensional Epithelial Morphogenesis in the Developing Drosophila Egg

“…Future work will be needed to address the molecular mechanisms by which patterns of tension are established. Included among the genes with patterned expression in the late follicular epithelium are several that encode proteins involved in cytoskeleton regulation or cell-cell adhesion (Dinkins et al, 2008; James et al, 2002; Jordan et al, 2005; Wahlström et al, 2006; Ward and Berg, 2005a; Yakoby et al, 2008; Zartman et al, 2009). Mutations in some of these genes result in dorsal appendage defects (Kleve et al, 2006; Laplante and Nilson, 2006; Zartman et al, 2008), but whether these genes work through regulating tension or through some other process has been largely unexplored.…”

Pattern formation by receptor tyrosine kinases: analysis of the Gurken gradient in Drosophila oogenesis

“…Recent studies of EGFR-mediated pattern formation in Drosophila oogenesis provided the first quantitative description of the GRK gradient [11••], began to elucidate the networks that interpret this gradient [12•,18,29••], and established a systems-level view of gene expression patterns in the follicular epithelium [29••,30,31]. These studies led to a number of mechanistic models which should be tested by the identification of m-regulatory modules of br and other transcriptional targets of EGFR signaling in the follicle cells.…”

Unit Operations of Tissue Development: Epithelial Folding

“…Epithelial structures that share a similarity in folding events would be expected in at least some cases to reflect conserved spatial relationships of gene expression. One indication that this may in fact be the case is the similar patterns of overlapping gene expression found in the formation of the larval posterior spiracles during embryogenesis and in defining the follicle cell domains (77, 80). The posterior spiracles are openings for the larval trachea and are also formed by invagination.…”

“…Cad74A is certainly not the only gene that must be patterned to generate the 3D eggshell structures (77). A current focus of investigation is the regulation of the functions of other candidate effectors of morphogenesis.…”

“…For example, it is clear that the vocabulary of human languages consists of only a small fraction of the possible combinations of letters. Similarly, only a small fraction of the total possible number of spatial patterns that can be constructed from the primitives in oogenesis are observed in screens of gene expression patterns (66, 77). …”