The repertoire of epithelial morphogenesis on display: Progressive elaboration of Drosophila egg structure

Abstract

Epithelial structures are foundational for tissue organization in all metazoans. Sheets of epithelial cells form lateral adhesive junctions and acquire apico-basal polarity perpendicular to the surface of the sheet. Genetic analyses in the insect model, Drosophila melanogaster, have greatly advanced our understanding of how epithelial organization is established, and how it is modulated during tissue morphogenesis. Major insights into collective cell migrations have come from analyses of morphogenetic movements within the adult follicular epithelium that cooperates with female germ cells to build a mature egg. Epithelial follicle cells progress through tightly choreographed phases of proliferation, patterning, reorganization and migrations, before they differentiate to form the elaborate structures of the eggshell. Distinct structural domains are organized by differential adhesion, within which lateral junctions are remodeled to further shape the organized epithelia. During collective cell migrations, adhesive interactions mediate supracellular organization of planar polarized macromolecules, and facilitate crawling over the basement membrane or traction against adjacent cell surfaces. Comparative studies with other insects are revealing the diversification of morphogenetic movements for elaboration of epithelial structures. This review surveys the repertoire of follicle cell morphogenesis, to highlight the coordination of epithelial plasticity with progressive differentiation of a secretory epithelium. Technological advances will keep this tissue at the leading edge for interrogating the precise spatiotemporal regulation of normal epithelial reorganization events, and provide a framework for understanding pathological tissue dysplasia.

Tissue tension and not interphase cell shape determines cell division orientation in the Drosophila follicular epithelium

“…Secondly, planar orientation in the wing disc, pupal notum, and embryonic mesectoderm is determined by cortical tension at the apical tissue surface (Mao et al, 2013;Bosveld et al, 2016;Wang et al, 2017). Cell shape is attributed to the collective cell migration that drives egg chamber rotation, which requires a traction force on basal cell surfaces (Haigo & Bilder, 2011;Cetera et al, 2014;Duhart et al, 2017;Viktorinová et al, 2017). Furthermore, the extent of individual cell elongation correlates strongly with this directional bias ( Fig EV2I).…”

A hormonal cue promotes timely follicle cell migration by modulating transcription profiles

“…Border cells form around two anterior polar cells, which are specified earlier, and the two different cell types adhere together to move between the large germline nurse cells and to reach the edge of the oocyte. Soon after border cell migration is completed, about 50 centripetal cells, located along the equator of the egg chamber, migrate internally to cover the anterior side of the oocyte (reviewed in (Dobens and Raftery, 2000; Duhart et al, 2017)). Centripetal cells move like an iris, spreading to close across the oocyte.…”

GAGA protein is required for multiple aspects of Drosophila oogenesis and female fertility

“…During normal oogenesis, between stages 9 and 11, the follicle cells undergo a series of morphological changes and cell migration that result in the oocyte becoming completely surrounded by follicle cells (Figure , Figure a,g) (reviewed in Spradling, ; Dobens & Raftery, ; Horne‐Badovinac & Bilder, ; Duhart, Parsons, & Raftery, ). Normally, a network of basal actin filaments is formed in these cells (Figure c).…”

“…At stage 10B the group of follicular cells migrate centripetally from the periphery of the egg chamber between the oocyte and the nurse cells (Figure ) to cover the anterior end of the oocyte (Figure g). These cells, known as centripetal cells, form a boundary between the oocyte and the nurse cells and later are involved in operculum formation (reviewed in Dobens & Raftery, ; Horne‐Badovinac & Bilder, ; Duhart et al, ).…”

“…It is known that the cytoplasmic actin of nurse cells is associated with rapid transport into the oocyte (Cooley & Theurkauf, ; Gutzeit, ), and the basal actin of follicular cells is necessary for egg chamber elongation (Gates, ). The border cells form a micropyle required for fertilization, and the centripetal cells form a cellular monolayer that restricts the oocyte from the nurse cells (for review see Duhart et al, ). Yolk granules are the main component of the egg required for subsequent embryogenesis.…”