Intercellular protein movement in syncytialDrosophilafollicle cells

Abstract

SummaryRing canals connecting Drosophila germline, follicle and imaginal disc cells provide direct contact of cytoplasm between cells. To date, little is known about the formation, structure, or function of the somatic ring canals present in follicle and imaginal disc cells. Here, we show by confocal and electron microscopy that Pavarotti kinesin-like protein and Visgun are stable components of somatic ring canals. Using live-cell confocal microscopy, we show that somatic ring canals form from the stabilization of mitotic cleavage furrows. In contrast to germline cells, syncytial follicle cells do not divide synchronously, are not maximally branched and their ring canals do not increase in size during egg chamber development. We show for the first time that somatic ring canals permit exchange of cytoplasmic proteins between follicle cells. These results provide insight into the composition and function of ring canals in somatic cells, implying a broader functional significance for syncytial organization of cells outside the germline.

Bridging the divide

“…A closer inspection of follicle cell divisions revealed a random mitotic spindle orientation with respect to existing RCs. 12 This, in combination with a stochastic closure of 10% of cleavage furrows, is consistent with the observed random configuration, orientation, and distribution of syncytium sizes within the epithelium.…”

“…12 Based on the wide range of sizes of these proteins and the work of others in characterizing diffusion rates in cytoplasm, 19 size does not seem to be a significant discriminating factor for movement through RCs. However, the FLIP analysis was restricted to less than 60 min, so movement of proteins or protein complexes that diffuse over the course of hours-potentially including the ribosomes-could be missed.…”

“…However, proteins that can diffuse (e.g., Cam, Oda, and Men-b) have uniform protein levels across the epithelium. 12 A possible explanation for this difference is that intercellular diffusion equilibrates the levels of proteins that are able to move through RCs; evidence of transcriptional variation between cells would provide compelling evidence of this model. Detecting subtle differences of transcript abundance in individual cells of an epithelium, however, represents a significant technical challenge.…”

“…12,13 The results suggest somatic RCs can provide cells with a mechanism to equilibrate protein levels and compensate for disparities in transcription between connected cells.…”

Germline and somatic vitelline proteins colocalize in aggregates in the follicular epithelium ofDrosophilaovaries

“…9 However, the aggregates of these two proteins did not colocalize with those of GFP::Pav-KLP, a ring canal marker. 12 In agreement with this observation, neither did we detect the colocalization of Polehole with Cindr (Fig. 1J), the Drosophila CD2AP/CIN85 ortholog and a component of somatic ring canals.…”