Cytoophidia safeguard binucleation of Drosophila male accessory gland cells

Although most cells of animal organs contain a single nucleus, a considerable number of cells are multinucleate. In some cases, multinucleation is the result of cell fusion (such as placental trophoblasts or skeletal muscle) or mitosis without cytokinesis (such as liver cells or muscle cells) during tissue/cell growth [[1], [2], [3]]. In this case, the numbers of chromosome copies and nuclei in each cell increase. In other tissue/cell growth situations, such as cell division and endoduplication, each cell has only one nucleus.

Previous scientific studies show that the binucleation of hepatocytes and muscle cells occurs during the individual growth period from lactation to weaning, and the proportion of binucleated cells in stem cells gradually increases, which has been proved to be mainly determined by nutritional signals [2]. In rat muscle cells, the formation of binuclear cells mainly occurs ten days after birth [1]. However, the factors affecting binucleation remain unclear.

CTP synthase (CTPS) is an important metabolic enzyme that catalyzes the rate-limiting step of de novo synthesis of the CTP nucleotide [4]. Since 2010, it has been found that CTPS forms filamentous structures called cytoophidia in all three domains of life, including archaea, bacteria, yeast, plants, fruit flies, zebrafish and mammals [[5], [6], [7], [36]]. Forming cytoophidia can affect enzymatic activity and prolong the half-life [[8], [9], [10]]. Cytoophidia may act as developmental switches. For example, cytoophidia disassemble upon reactivation of developmentally arrested neuroblasts in Drosophila larvae [11]. In C. crescentus, CTPS filaments cooperate with the intermediate filament CreS to maintain cell shape [12]. Moreover, disrupting cytoophidium formation impairs adipocyte adhesion and tissue architecture [13].

Cytoophidia are observed in different cell types of Drosophila, including cells in male reproductive system [14]. It is well known that the epithelial cells of the male accessory gland (MAG) are binucleate [15]. However, it is not clear whether cytoophidia play a role in binucleation.

Drosophila melanogaster is a powerful tool to study human diseases, metabolism, development, innate immunity, and energy homeostasis. MAG of Drosophila and humans have similar tissues, anatomical structures and physiological functions [16]. The main cells of MAG of Drosophila provide an attractive system for studying the binuclear function of cytoophidia.

MAG is a tubular or spherical exocrine organ of internal reproductive system of insects. Its location and function are similar to those of the mammalian prostate [17]. MAG produces and secretes components in sperm plasma, which fuse with sperm during mating and enter female copulatory sac. The epithelial cells of Drosophila MAG are composed of two types of cells: approximately 1000 polygonal “main cells” and 40 spherical “secondary cells”. Both types of cells have two nuclei. The binuclear system changes its apical-basal position from vertical to horizontal relative to the epithelial plane, so that the apical region of each cell has higher plasticity, thus producing a large volume of semen [18]. Defective proventriculus (Dve), which is enriched in secondary cells, is required for accessory gland development, binucleation of main cells, survival of secondary cells, and male fecundity [19]. Main cells secrete abundant accessory gland proteins, including sex peptides, which are crucial for male fertility [20,21].

It is well known that substances produced by MAG play several important roles in male reproductive success. One is that the secretion of fluid provides sperm nutrition, promotes the continued development and maturation of sperm, and enhances its vitality [22]. The second role is to regulate female reproductive behavior, such as feeding, oviposition, and refusal to mate with other males, which has been elaborated by the genetically compatible insect Drosophila melanogaster. In the case of Drosophila, individuals with larger MAG volumes show higher reproductive capacity [23,24].

The MAG of Drosophila plays a very important role in its reproduction. We find that most of the main cells of the Drosophila MAG lacking cytoophidia cannot form binucleate cells, and the presence of such mononuclear cells has no direct relationship with CTPS protein level. Our data suggest that cytoophidia play a key role in the formation of binuclear cells.

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