DYNAMICS OF COLLECTIVE GROWTH IN THE DROSOPHILA GERMLINE

Abstract

Developing oocytes need large supplies of macromolecules and organelles. A conserved strategy for accumulating these products is to pool resources of oocyte-associated nurse cells. In Drosophila, these cells grow more than 100-fold to boost their biosynthetic capacity. No previously known mechanism explains how nurse cells coordinate growth collectively. In this thesis I report a cell cycle-regulating mechanism that depends on bidirectional communication between the oocyte and nurse cells, revealing the oocyte as a critical regulator of germline cyst growth. Transcripts encoding the Cyclin-dependent kinase inhibitor Dacapo are synthesized by the nurse cells and actively localized to the oocyte. Retrograde movement of oocyte-synthesized Dacapo protein to the nurse cells generates a network of coupled oscillators that controls the cell cycle of the nurse cells to regulate cyst growth. I propose that bidirectional nurse cell-oocyte communication establishes a growth sensing feedback mechanism that regulates the quantity of maternal resources loaded into the oocyte. Furthermore, the nurse cells are not the only cells that engage in bidirectional communication with the oocyte. I present preliminary findings on how the mechanical properties of the cytoskeleton in the germline and overlying somatic follicle cells may coordinate growth of these two tissues. Finally, I expand on these experimental findings to discuss comparisons between Drosophila and mouse oogenesis and propose that bidirectional communication between oocytes and support cells is a universal feature of oogenesis across species.