The Drosophila male accessory gland has functions similar to those of the mammalian prostate gland and the seminal vesicle, and secretes accessory gland proteins into the seminal fluid. Each of the two lobes of the accessory gland is composed of two types of binucleate cell: about 1,000 main cells and 40 secondary cells. A well-known accessory gland protein, sex peptide, is secreted from the main cells and induces female postmating response to increase progeny production, whereas little is known about physiological significance of the secondary cells. The homeodomain transcriptional repressor Defective proventriculus (Dve) is strongly expressed in adult secondary cells, and its mutation resulted in loss of secondary cells, mononucleation of main cells, and reduced size of the accessory gland. dve mutant males had low fecundity despite the presence of sex peptide, and failed to induce the female postmating responses of increased egg laying and reduced sexual receptivity. RNAi-mediated dve knockdown males also had low fecundity with normally binucleate main cells. We provide the first evidence that secondary cells are crucial for male fecundity, and also that Dve activity is required for survival of the secondary cells. These findings provide new insights into a mechanism of fertility/fecundity.
BackgroundIn standard cell division, the cells undergo karyokinesis and then cytokinesis. Some cells, however, such as cardiomyocytes and hepatocytes, can produce binucleate cells by going through mitosis without cytokinesis. This cytokinesis skipping is thought to be due to the inhibition of cytokinesis machinery such as the central spindle or the contractile ring, but the mechanisms regulating it are unclear. We investigated them by characterizing the binucleation event during development of the Drosophila male accessory gland, in which all cells are binucleate.ResultsThe accessory gland cells arrested the cell cycle at 50 hours after puparium formation (APF) and in the middle of the pupal stage stopped proliferating for 5 hours. They then restarted the cell cycle and at 55 hours APF entered the M-phase synchronously. At this stage, accessory gland cells binucleated by mitosis without cytokinesis. Binucleating cells displayed the standard karyokinesis progression but also showed unusual features such as a non-round shape, spindle orientation along the apico-basal axis, and poor assembly of the central spindle. Mud, a Drosophila homolog of NuMA, regulated the processes responsible for these three features, the classical isoform MudPBD and the two newly characterized isoforms MudL and MudS regulated them differently: MudL repressed cell rounding, MudPBD and MudS oriented the spindle along the apico-basal axis, and MudS and MudL repressed central spindle assembly. Importantly, overexpression of MudS induced binucleation even in standard proliferating cells such as those in imaginal discs.ConclusionsWe characterized the binucleation in the Drosophila male accessory gland and examined mechanisms that regulated unusual morphologies of binucleating cells. We demonstrated that Mud, a microtubule binding protein regulating spindle orientation, was involved in this binucleation. We suggest that atypical functions exerted by three structurally different isoforms of Mud regulate cell rounding, spindle orientation and central spindle assembly in binucleation. We also propose that MudS is a key regulator triggering cytokinesis skipping in binucleation processes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12861-014-0046-5) contains supplementary material, which is available to authorized users.
Although most animal cells possess only a single nucleus, some cells such as myocytes and hepatocytes show sporadic occurrences of multiple nuclei. The Drosophila adult male accessory gland, an internal reproductive organ for production of seminal fluid components, displays an exceptional columnar epithelium where all cells have two nuclei. Despite this striking feature, no adaptive significances to account for binucleation have been proposed.We demonstrate that one possible purpose of binucleation is enabling plasticity in organ size. To compare various cytological traits between binucleate and mononucleate states, we artificially converted the cellular state from the binucleate state to either the endoreplicated mononucleate or pseudodivided mononucleate state in the accessory gland epithelium by genetically manipulating the spindle assembly checkpoint. Depending on the flies' age and mating and feeding conditions, the apical area of the binucleate cells enlarges compared with that of endoreplicated mononucleate cells. On the other hand, the apical area shrinks after mating compared with that of divided mononucleate cells. Consequently, this wide range of apical area size in binucleate cells increases the plasticity in organ size compared with that in endoreplicated mononucleate and divided mononucleate cells. The highly plastic features in an organ composed of binucleate cells should lead to higher rates of reproductive success in response to nutrition uptake and mating frequency. Similar plasticity might also be beneficial in hepatocytes and myocytes, both of which show great variability in cell size. Our results provide direct evidence that cell-size plasticity is a basis of multinucleation in animal cells.
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