Coordinating Proliferation, Polarity, and Cell Fate in the Drosophila Female Germline

Abstract

Gametes are highly specialized cell types produced by a complex differentiation process. Production of viable oocytes requires a series of precise and coordinated molecular events. Early in their development, germ cells are an interconnected group of mitotically dividing cells. Key regulatory events lead to the specification of mature oocytes and initiate a switch to the meiotic cell cycle program. Though the chromosomal events of meiosis have been extensively studied, it is unclear how other aspects of oocyte specification are temporally coordinated. The fruit fly, Drosophila melanogaster, has long been at the forefront as a model system for genetics and cell biology research. The adult Drosophila ovary continuously produces germ cells throughout the organism's lifetime, and many of the cellular processes that occur to establish oocyte fate are conserved with mammalian gamete development. Here, we review recent discoveries from Drosophila that advance our understanding of how early germ cells balance mitotic exit with meiotic initiation. We discuss cell cycle control and establishment of cell polarity as major themes in oocyte specification. We also highlight a germline-specific organelle, the fusome, as integral to the coordination of cell division, cell polarity, and cell fate in ovarian germ cells. Finally, we discuss how the molecular controls of the cell cycle might be integrated with cell polarity and cell fate to maintain oocyte production.

Loss of Drosophila E3 Ubiquitin Ligase Hyd Promotes Extra Mitosis in Germline Cysts and Massive Cell Death During Oogenesis

“…According to our results, the death of Hyd-deficient GCs in nanos-GAL4/UAS-hyd-RNAi ovaries begins in late third instar larvae. The ovaries at this stage contain primordial germ cells (PGCs) that terminate to divide and specialize in two directions: several cells interact with a newly formed niche and become germline stem cells, whereas the remaining cells begin to differentiate and become cystoblasts (Gancz et al, 2011;Kahney et al, 2019;Hinnant et al, 2020). Germline differentiation factor Bam governs both stem cell maintenance and the differentiation of their progeny: Bam expression is inhibited in stem cells (where differentiation is prohibited) and activated in cystoblasts (where differentiation is promoted) (Ji et al, 2017;Mathieu and Huynh, 2017;Kahney et al, 2019).…”

Drosophila p53isoforms have overlapping and distinct functions in germline genome integrity and oocyte quality control

“…Given that endocycling nurse cells and the meiotic oocyte repress p53 apoptosis, we analyzed the apoptotic response of mitotically-dividing germline cells during early oogenesis in the germarium (Mehrotra et al 2008;Hassel et al 2014;Zhang et al 2014;Qi and Calvi 2016). At the anterior tip of the germarium, the germline stem cells (GSCs) reside in a niche and divide asymmetrically into a GSC and cystoblast (CB) ( Figure 3A) (Hinnant et al 2020). This cystoblast and its daughter cells undergo four rounds of divisions with incomplete cytokinesis as they migrate posteriorly through germarium region 1, finally resulting in an interconnected 16-cell germline cyst.…”

“…This cystoblast and its daughter cells undergo four rounds of divisions with incomplete cytokinesis as they migrate posteriorly through germarium region 1, finally resulting in an interconnected 16-cell germline cyst. ( Figure 3A) (Drummond-Barbosa 2019; Hinnant et al 2020). In region 2a, multiple cells in the cyst initiate meiotic breaks and synaptonemal complex formation, but only one cell is eventually specified to be the oocyte, with the 15 other cells of the cyst destined to become nurse cells that enter a polyploid endocycle by germarium region 3 (stage 1 of oogenesis) ( Figure 3A).…”

HtsRC-Mediated Accumulation of F-Actin Regulates Ring Canal Size During Drosophila melanogaster Oogenesis

“…In Drosophila, oogenesis occurs in egg chambers, the functional units of the ovary. Each egg chamber contains a syncytium of 16 germline cells: 15 nurse cells and one transcriptionally quiescent oocyte, formed through four rounds of mitosis via incomplete cytokinesis (HINNANT et al 2020).…”