Differential soma-germline affinity controls drosophila oogenesis

Abstract: It is well established that the development of oocytes is strictly dependent on close soma-germline interaction. Although signaling between germline and soma has been studied, the joint morphogenesis is only poorly understood. During oogenesis, a somatic epithelium envelopes the developing germline and cooperatively they undergo defined morphological changes to ensure oocyte maturation. Remarkably, the contact surface between germline and epithelium is established by the apical surface of epithelial cells. The epithelial apical surface is therefore in the unusual situation of engaging in direct cell-cell contact and establishes an interface between two cell lineages. While this special interface must play a crucial role in coordinating the joint morphogenesis of germline and epithelium, only little is known about its mechanical properties.
We used Drosophila egg chamber development, a well-established model system, to study soma-germline interface dynamics during oogenesis. The developing egg chamber consists of a germline cyst comprised of 15 nurse cells and 1 oocyte, and a monolayer epithelium enveloping the germline cyst. Egg chambers have to undergo several processes during development that are highly dependent on the tight coordination of germline and epithelium. Yet, to date the direct cell-cell interface between germline and epithelium has been neglected in studies of egg chamber morphogenesis. Employing extensive quantitative description of egg chamber morphogenesis, functional genetic studies and mathematical modeling, we were able to uncover a simple mechanical mechanism that controls the interaction of epithelium and germline throughout egg chamber development. We propose that differential interfacial tension between epithelial cells and germline cells drives egg chamber morphogenesis. We identified Eya as a master regulator of epithelial cell affinity towards germline cells and show that the dynamic expression patterns of Eya throughout egg chamber development control follicle cell shape and distribution. Furthermore, we demonstrated that the morphology of the germline cyst is controlled by the Eya-regulated affinity between epithelial cells and germline. Thus, our studies demonstrate that the mechanical properties of the interface between germline and epithelium drive egg chamber morphogenesis.
Furthermore, we describe a reorganization of the epithelial apical cortex and propose that the shift of contractility from the adherens junctions into the apical cortex, in combination with corrugated adherens junctions mechanically uncouples cells within the epithelium. We hypothesize that this disconnection within the epithelium maintains epithelial integrity, while facilitating the coexistence of mechanically different epithelial subpopulations and the accommodation of tensile forces from the growing germline.
These studies provide a simple mechanical principle as the driving force of Drosophila egg chamber development and thereby provide a mechanism that enables the morphological coordination of cell lineages. Our findings describe mechanical principles that are likely not unique to egg chamber morphogenesis and instead rather provide insights into how tissues interact with each other and especially how epithelia engage in complex morphogenetic processes

Object Details

• Location: Deutsche Nationalbibliothek Frankfurt am Main
• Extent: Online-Ressource
• Language: Englisch
• Notes: Universität Freiburg, Dissertation, 2022

Classification and Topics

• Keyword: Epithelzelle ; Zellkontakt ; Zelladhäsion ; Actin-Filament ; Zellskelett

Contributors, Places and Time

• Event: Veröffentlichung
• (where): Freiburg
• (who): Universität
• (when): 2022
• Creator: Weichselberger, Vanessa
• Contributor: Claßen, Anne-Kathrin ; Claßen, Anne-Kathrin ; Pyrowolakis, George ; Albert-Ludwigs-Universität Freiburg. Fakultät für Biologie ; Professur für Entwicklungsbiologie der Tiere

Further information

• DOI: 10.6094/UNIFR/226769
• URN: urn:nbn:de:bsz:25-freidok-2267699
• Rights: Open Access; Der Zugriff auf das Objekt ist unbeschränkt möglich.
• Last update: 25.03.2025, 1:54 PM CET