Septate junction proteins are required for egg elongation and border cell migration during oogenesis in Drosophila

Abstract

Protein components of the invertebrate occluding junction—known as the septate junction (SJ) - are required for morphogenetic developmental events during embryogenesis in Drosophila melanogaster. In order to determine whether SJ proteins are similarly required for morphogenesis during other developmental stages, we investigated the localization and requirement of four representative SJ proteins during oogenesis: Contactin, Macroglobulin complement-related, Neurexin IV, and Coracle. A number of morphogenetic processes occur during oogenesis, including egg elongation, formation of dorsal appendages, and border cell migration. We found that all four SJ proteins are expressed in egg chambers throughout oogenesis, with the highest and most sustained levels in the follicular epithelium (FE). In the FE, SJ proteins localize along the lateral membrane during early and mid-oogenesis, but become enriched in an apical-lateral domain (the presumptive SJ) by stage 10B. SJ protein relocalization requires the expression of other SJ proteins, as well as Rab5 and Rab11 in a manner similar to SJ biogenesis in the embryo. Knocking down the expression of these SJ proteins in follicle cells throughout oogenesis results in egg elongation defects and abnormal dorsal appendages. Similarly, reducing the expression of SJ genes in the border cell cluster results in border cell migration defects. Together, these results demonstrate an essential requirement for SJ genes in morphogenesis during oogenesis, and suggests that SJ proteins may have conserved functions in epithelial morphogenesis across developmental stages. Article Summary: Septate junction (SJ) proteins are essential for forming an occluding junction in epithelial tissues in Drosophila melanogaster, and also for morphogenetic events that occur prior to the formation of the junction during embryogenesis. Here we show that SJ proteins are expressed in the follicular epithelium of egg chambers during oogenesis and are required for morphogenetic events including egg elongation, dorsal appendages formation, and border cell migration. Additionally, the formation of SJs during oogenesis is similar to that in embryonic epithelia.

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

“…However, small septate junctions appear during stage 8 when broad protrusions of the oocyte and follicle cell membranes become in contact. This finding is unexpected since septate junctions have been described in the Drosophila egg chambers, but they only assemble by stage 6 between adjacent follicle cells [ 30 , 40 , 41 , 42 ]. Moreover, these contacts represent an intriguing exception since the septate junction is usually found at the apical-lateral region of adjacent cells of the same tissue and are stable contacts that usually persist during the cell life.…”

Transcriptome analysis reveals temporally regulated genetic networks duringDrosophilaborder cell collective migration

“…These migration-related activities included regulation of the cytoskeleton, cell adhesion, small GTPase activity, and cell polarity. Cluster C0 had additional functional interaction modules with proteins required for septate junction formation and proteins involved in ecdysone signaling response, both of which are required for border cell migration ( Figure 4A ) [53; 25; 27; 54]. Cluster C8 was further enriched with modules of proteins with annotated broad functions in development, including cell signaling, serine-threonine kinase activities, and regulation of gene expression ( Figure 4C ).…”

“…Similarly, border cells require complex regulation of cell-cell adhesions for their collective migration to maintain cluster integrity and shape as well as to migrate on and between nurse cells [20; 67; 19; 23; 6]. Recent genetic screens and targeted approaches have uncovered various adhesion genes, including septate junction genes, that promote border cell collective cohesion and migration [53; 70; 23]. Consistent with this, we observed a broad pattern of dynamic adhesion-related gene expression from early- to late-migration stages.…”

The Lipid Phosphate Phosphatase Wunen Promotes Eggshell Formation and Is Essential for Fertility in Drosophila

“…Follicle cells are also polarised epithelial cells and also express septate junction components. Follicle cell septate junction components localise along the entire lateral membrane until stage 11 [30][31][32] and only become apicolateral restricted late in oogenesis [33]. Incipient SJs between follicle cells form as early as in stage 6 egg chambers, but typical pleated SJs are only observed from stage 10 onwards [34,35], as reviewed in [36].…”