Animal oocytes undergo a highly conserved developmental arrest in prophase of meiosis I. Often this marks a period of rapid growth for the oocyte and is necessary to coordinate meiotic progression with the developmental events of oogenesis. In Drosophila, the oocyte develops within a 16-cell germline cyst. Throughout much of oogenesis, the oocyte remains in prophase of meiosis I. By contrast, its 15 mitotic sisters enter the endocycle and become polyploid in preparation for their role as nurse cells. How germline cysts establish and maintain these two independent cell cycles is unknown. We demonstrate a role for the p21 CIP /p27 Kip1 /p57 Kip2 -like cyclin-dependent kinase inhibitor (cki) dacapo in the maintenance of the meiotic cycle in Drosophila oocytes. Our data indicate that it is through the differential regulation of the cki Dacapo that two modes of cell-cycle regulation are independently maintained within the common cytoplasm of ovarian cysts.
Drosophila ovarian cysts arise through a series of four synchronous incomplete mitotic divisions. After each round of mitosis, a membranous organelle, the fusome, grows along the cleavage furrow and the remnants of the mitotic spindle to connect all cystocytes in a cyst. The fusome is essential for the pattern and synchrony of the mitotic cyst divisions as well as oocyte differentiation. Using live cell imaging, greenfluorescent protein-tagged proteins, and photobleaching techniques, we demonstrate that fusomal endomembranes are part of a single continuous endoplasmic reticulum (ER) that is shared by all cystocytes in dividing ovarian cysts. Membrane and lumenal proteins of the common ER freely and rapidly diffuse between cystocytes. The fusomal ER mediates intercellular ER connectivity by linking the cytoplasmic ER membranes of all cystocytes within a cyst. Before entry into meiosis and onset of oocyte differentiation (between region 1 and region 2A), ER continuity between cystocytes is lost. Furthermore, analyses of hts and Dhc64c mutants indicate that intercellular ER continuity within dividing ovarian cysts requires the fusome cytoskeletal component and suggest a possible role for the common ER in synchronizing mitotic cyst divisions. INTRODUCTIONGametogenesis takes place within germline cysts in a wide array of organisms (Telfer, 1975;Bü ning, 1994;de Cuevas et al., 1997). In Drosophila a single oocyte develops within the environment of a 16-cell cyst. The development of this cyst occurs in a series of morphologically defined regions (see Figure 1A). Cyst production begins when a germline stem cell divides asymmetrically to produce a cystoblast. The cystoblast undergoes four synchronous mitotic divisions (regions 1 and 2a), with incomplete cytokinesis, to produce a cluster of 16 cells that are connected via arrested mitotic cleavage furrows (reviewed in de Cuevas et al., 1997). Later in oogenesis, the arrested cleavage furrows mature into stable ring canals and are reinforced with an actin cytoskeleton (reviewed in Mahajan-Miklos and Cooley, 1994). Initially, all 16 cystocytes develop in synchrony. However, as development proceeds, differentiation within the cyst becomes asynchronous. Ultimately, only one cell commits to meiosis and differentiates as the oocyte, whereas the other 15 cystocytes enter the endocycle and develop as trophic nurse cells.A unique membranous organelle, the fusome, grows and branches along the spindle equators after each mitotic division to physically connect all cells within a cyst. The fusome is found in the germline cysts of Drosophila as well as other insects (reviewed in Telfer, 1975;McKearin, 1997). The Drosophila fusome is comprised of cytoplasmic endomembranes, membrane skeletal proteins and polarized microtubules (reviewed in de Cuevas et al., 1997;McKearin, 1997).Molecular genetic studies over the last ten years indicate the fusome mediates several essential steps in germline cyst development (reviewed in McKearin, 1997). The differentiation of the oocyte depends on the pr...
In Drosophila, a single oocyte develops within a 16-cell germline cyst. Although all 16 cells initiate meiosis and undergo premeiotic S phase,only the oocyte retains its meiotic chromosome configuration and remains in the meiotic cycle. The other 15 cells in the cyst enter the endocycle and develop as polyploid nurse cells. A longstanding goal in the field has been to identify factors that are concentrated or activated in the oocyte, that promote meiotic progression and/or the establishment of the oocyte identity. We present the characterization of the missing oocyte gene, an excellent candidate for a gene directly involved in the differentiation of the oocyte nucleus. The missing oocyte gene encodes a highly conserved protein that preferentially accumulates in pro-oocyte nuclei in early prophase of meiosis I. In missing oocyte mutants, the oocyte enters the endocycle and develops as a polyploid nurse cell. Genetic interaction studies indicate that missing oocyte influences meiotic progression prior to pachytene and may interact with pathways that control DNA metabolism. Our data strongly suggest that the product of the missing oocyte gene acts in the oocyte nucleus to facilitate the execution of the unique cell cycle and developmental programs that produce the mature haploid gamete.
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