Cell-to-Cell Interactions during Early Drosophila Oogenesis: An Ultrastructural Analysis

Abstract

Drosophila oogenesis requires the subsequent growth of distinct egg chambers each containing a group of sixteen germline cells surrounded by a simple epithelium of follicle cells. The oocyte occupies a posterior position within the germ cells, thus giving a distinct asymmetry to the egg chamber. Although this disposition is critical for the formation of the anterior–posterior axis of the embryo, the interplay between somatic and germ cells during the early stages of oogenesis remains an open question. We uncover by stage 2, when the egg chambers leaved the germarium, some unique spatial interactions between the posterior follicle cells and the oocyte. These interactions are restricted to the surface of the oocyte over the centriole cluster that formed during early oogenesis. Moreover, the posterior follicle cells in front of the oocyte display a convoluted apical membrane with extensive contacts, whereas the other follicle cells have a flat apical surface without obvious surface protrusions. In addition, the germ cells located at the posterior end of the egg chamber have very elongated protrusions that come into contact with each other or with facing follicle cells. These observations point to distinct polarization events during early oogenesis supporting previous molecular data of an inherent asymmetry between the anterior and the posterior regions of the egg chambers.

Homophilic interaction of E-Cadherin prevents cell-cell fusion between developing germline and surrounding epithelia inDrosophilaovary

“…Tight membrane attachment was also observed in NC-NC boundaries and FC-FC boundaries throughout the stages (Figure 1F, G). At all stages analyzed, we observed adherens junctions between FCs (Figure 1G, asterisk) as reported previously [36,37], and unique membrane processes between oocytes and NCs or between oocytes and FCs (Figure 1H, I) as reported recently [22].…”

“…However, it is unclear whether E-Cadherin is involved in interactions between these cell types. In early ultrastructural studies, no clear junction is identified in these cell types [1][2][3]22]. E-Cadherin has been also found to localize outside of the junction, known as non-junctional Cadherin [23][24][25][26][27], suggesting that E-Cadherin may also play a role without forming junctions.…”

The Importance of the Position of the Nucleus in Drosophila Oocyte Development

“…For several years, it was thought the Drosophila oocyte lacked active centrosomes at stages where nuclear migration occurred, as suggested by the failure to detect them during early oocyte development [49] and by the fact that the meiotic spindle formed in the absence of centrosomes at the end of oogenesis [50]. More recently, several studies have documented the existence of active centrosomes during oocyte development [16,18,24,51]. As mentioned above, the oocyte contains at least 16 centrosomes that come together to form a cluster.…”

Lineage-based scaling of germline intercellular bridges during oogenesis

“…Alternatively, if the M1 contractile ring constricts less than contractile rings formed in subsequent divisions, perhaps it must be reinforced by the recruitment of more actin filaments or stabilized by additional cell-cell junctions, which may impact growth. Extensive cell-cell contacts have been observed in the developing germ cell cysts (Loyer et al, 2015;Riparbelli et al, 2022;Tilney et al, 1996), but a comparison of their distribution within different regions of the germ cell cluster has not been performed. One final explanation we considered is that the growth of a posterior ring canal could depend on how many other ring canals exist within that germ cell.…”