Symmetry Breaking During Drosophila Oogenesis

Abstract

The orthogonal axes of Drosophila are established during oogenesis through a hierarchical series of symmetry-breaking steps, most of which can be traced back to asymmetries inherent in the architecture of the ovary. Oogenesis begins with the formation of a germline cyst of 16 cells connected by ring canals. Two of these 16 cells have four ring canals, whereas the others have fewer. The first symmetry-breaking step is the selection of one of these two cells to become the oocyte. Subsequently, the germline cyst becomes surrounded by somatic follicle cells to generate individual egg chambers. The second symmetry-breaking step is the posterior positioning of the oocyte within the egg chamber, a process mediated by adhesive interactions with a special group of somatic cells. Posterior oocyte positioning is accompanied by a par gene-dependent repolarization of the microtubule network, which establishes the posterior cortex of the oocyte. The next two steps of symmetry breaking occur during midoogenesis after the volume of the oocyte has increased about 10-fold. First, a signal from the oocyte specifies posterior follicle cells, polarizing a symmetric prepattern present within the follicular epithelium. Second, the posterior follicle cells send a signal back to the oocyte, which leads to a second repolarization of the oocyte microtubule network and the asymmetric migration of the oocyte nucleus. This process again requires the par genes. The repolarization of the microtubule network results in the transport of bicoid and oskar mRNAs, the anterior and posterior determinants, respectively, of the embryonic axis, to opposite poles of the oocyte. The asymmetric positioning of the oocyte nucleus defines a cortical region of the oocyte where gurken mRNA is localized, thus breaking the dorsal-ventral symmetry of the egg and embryo.

The developmental origins of the mammalian ovarian reserve

“…Furthermore, this work posits that each cyst present at the time of meiotic onset produces a single oocyte, which is quite similar to dynamics of oocyte and nurse cell production in Drosophila. Importantly, however, mammalian cysts are fragmented completely early in development, with the ovary possessing only intact follicles during adulthood (Lei and Spradling, 2013b); this is in contrast to Drosophila cysts, which are formed and utilized throughout the life of the animal (Roth and Lynch, 2009). Interestingly, it was also demonstrated that mouse oocytes possess a Balbiani body, or mitochondrial cloud of organelles localized next to the developing oocyte nucleus .…”

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

“…Similar to C. elegans, D. melanogaster also uses actin for embryonic polarization, however, the cue in this case is not sperm entry but inductive signaling and asymmetric transport of maternal mRNAs during oogenesis-there is no evidence for anterior-directed contractile cortical flow; reviewed in [273,274]. The cortical actin network is however directly responsible for localization of the polarity factor Par1 [275] and together with polarized localization of the polarity regulator Cdc42 involved in oocyte polarization through positive feedback onto the Par3/Par6/aPKC polarity complex [276].…”

The evolution of dorsal–ventral patterning mechanisms in insects

“…Since the Drosophila DV patterning gene regulatory network (GRN) is the gold standard to which other insects will be compared, crucial aspects of the functioning of this network are described here (for more in depth review, see Roth 2003; Moussian and Roth 2005;Hong et al 2008;Roth and Lynch 2009). The cascade of molecular interactions that lead to the establishment of cell fates along the DV axis of the Drosophila embryo begins with a symmetry-breaking event in the ovary, when the oocyte nucleus moves to a cortical position that is asymmetric with regard to the short axis of the egg chamber (Roth and Lynch 2009).…”

“…The cascade of molecular interactions that lead to the establishment of cell fates along the DV axis of the Drosophila embryo begins with a symmetry-breaking event in the ovary, when the oocyte nucleus moves to a cortical position that is asymmetric with regard to the short axis of the egg chamber (Roth and Lynch 2009). mRNA for gurken (grk) is localized around the oocyte nucleus and translated, and its protein (encoding a tgf-a-like EGF ligand) is secreted to the overlying somatic follicle cells, where it activates the EGF receptor (EGFR) ( Fig.…”