Occluding Junctions in Tissue Morphogenesis: Roles for Septate Junction Proteins in Drosophila melanogaster Egg Morphogenesis

Abstract

Tissue morphogenesis underlies many developmental processes in multicellular organisms and is essential for the basic organization of tissues and organs. Several cellular processes contribute to morphogenesis, including cell shape changes, cellular rearrangements, and cell movement. These morphological processes are regulated via protein trafficking and secretion, the cell cytoskeleton, and propagation of mechanical forces within cells and across tissues. In Drosophila, components of the invertebrate occluding junction, known as the septate junction (SJ), are required for several morphogenetic events during the embryonic and larval stages. Recent studies revealed a non-occluding functional requirement for SJ proteins in tissue morphogenesis during embryogenesis. However, whether a similar requirement is present in the adult tissue of the fly remains unknown. To explore this question, we used the Drosophila egg chamber as a model system. In Chapter II, we examined the expression pattern of four SJ proteins (Macroglobulin complement-related (Mcr), Contactin, Neuraxin IV, and Coracle) in the egg chambers throughout oogenesis. The examined SJ proteins localize along the lateral membrane of the follicle cells (FCs) of early-stage egg chambers but become enriched at the apical-lateral membrane in late-stage egg chambers, where they form the SJ. In addition, we determined that the re-localization event of SJ proteins in the follicular epithelium requires Rab5-mediated endocytosis and Rab11-mediated recycling. Next, we examined the role of SJ proteins in egg morphogenesis. We find that SJ proteins are required for morphogenetic events during oogenesis, including border cell migration, egg elongation, and the formation of the dorsal appendages. To further examine the cellular mechanism by which SJ proteins are required for egg morphogenesis, we focused our analysis on the role of Mcr in egg elongation. In Chapter III, we show that Mcr is required for egg elongation late in oogenesis. This requirement is mediated via maintaining a monolayered epithelium and cell-extracellular matrix adhesion. We also show that Mcr is required for eggshell layers formation, including the wax and chorion layers. The findings in this study set the foundation for the SJ field to study the role of SJ proteins in morphogenesis in post-embryonic epithelia and indicate a conserved role for SJ proteins in morphogenesis.