The cell adhesion molecules Echinoid and Friend of Echinoid coordinate cell adhesion and cell signaling to regulate the fidelity of ommatidial rotation in theDrosophilaeye

Abstract

Directed cellular movements are a universal feature of morphogenesis in multicellular organisms. Differential adhesion between the stationary and motile cells promotes these cellular movements to effect spatial patterning of cells. A prominent feature of Drosophila eye development is the 90°rotational movement of the multicellular ommatidial precursors within a matrix of stationary cells. We demonstrate that the cell adhesion molecules Echinoid (Ed) and Friend of Echinoid (Fred) act throughout ommatidial rotation to modulate the degree of ommatidial precursor movement. We propose that differential levels of Ed and Fred between stationary and rotating cells at the initiation of rotation create a permissive environment for cell movement, and that uniform levels in these two populations later contribute to stopping the movement. Based on genetic data, we propose that ed and fred impart a second, independent, 'brake-like' contribution to this process via Egfr signaling. Ed and Fred are localized in largely distinct and dynamic patterns throughout rotation. However, ed and fred are required in only a subset of cells -photoreceptors R1, R7 and R6 -for normal rotation, cells that have only recently been linked to a role in planar cell polarity (PCP). This work also provides the first demonstration of a requirement for cone cells in the ommatidial rotation aspect of PCP. ed and fred also genetically interact with the PCP genes, but affect only the degree-of-rotation aspect of the PCP phenotype. Significantly, we demonstrate that at least one PCP protein, Stbm, is required in R7 to control the degree of ommatidial rotation.

Echinoid regulates Flamingo endocytosis to control ommatidial rotation in theDrosophilaeye

“…6C). The dynamic and differential expression of Ed (and of its paralog Friend of Echinoid) in the rotating clusters and non-rotating ICs has also been proposed to modulate ommatidial rotation (Fetting et al, 2009). Thus, differential expression of Ed, Fmi, DE-cad and Friend of Echinoid in the rotating clusters and non-rotating ICs prevents the homotypic interaction of these four CAMs to allow free rotation of photoreceptor clusters.…”

“…Fetting et al recently showed that ed genetically interacts with Egfr pathway members, and proposed that ed, via inhibiting Egfr signaling in the photoreceptors, regulates ommatidial rotation (Fetting et al, 2009). However, we demonstrated that, after row 2, Ed facilitates the endocytosis of Egfr only in the non-rotating ICs, but not in the photoreceptor clusters (Fig.…”

“…3D) (J.-C.H., unpublished). As ed affects the levels of all the core PCP proteins tested in ICs, it remains unclear how ed only interacts genetically with the R3-specific PCP genes to modulate the degree of ommatidial rotation (Fetting et al, 2009). Finally, ed also weakly affects the initial R3/R4 specification, as a small proportion of ed mutant cells also show randomized chirality and symmetrical ommatidia.…”

Planar Cell Polarity Signaling in the Drosophila Eye

“…Indeed, two additional cell adhesion molecules, the IgCAM Echinoid (Ed), capable of homophilic and heterophilic interactions (Islam et al ., 2003), as well as its paralog Fred (Friend of Echinoid), have recently been described to be required for proper rotation (Fetting et al ., 2009; Ho et al ., 2010). While loss of their function causes a wide variation in the rotation angle of individual ommatidia, genetic interactions showed that ed and fred antagonistically interact with the EGFR signaling components pointed and canoe (Fetting et al ., 2009).…”

“…While loss of their function causes a wide variation in the rotation angle of individual ommatidia, genetic interactions showed that ed and fred antagonistically interact with the EGFR signaling components pointed and canoe (Fetting et al ., 2009). Ed is a known inhibitor of EGFR signaling in other contexts (Bai et al ., 2001), but enhances rotation defects of pnt and cno (Fetting et al ., 2009). In contrast, fred mutations suppress loss of cno or pnt , again pointing toward a tight interplay between EGFR signaling, cell adhesion, and rotation.…”