Cell-type-specific interacting proteins collaborate to regulate the timing of Cyclin B protein expression in male meiotic prophase.

During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes upregulate over 1800 genes and grow 25-fold. Previous work has shown that the cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here, we show that the spermatocyte-specific protein Lut is required for translational repression of cycB in an 8-h window just before spermatocytes are fully mature. In males mutant for rbp4 or lut, spermatocytes enter and exit meiotic division 6-8 h earlier than in wild type. In addition, spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein in mature spermatocytes and normal entry into the meiotic divisions. Lut and Syp interact with Fest independent of RNA. Thus, a set of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase.

A cell-type-specific multi-protein complex regulates expression of Cyclin B protein in Drosophila male meiotic prophase.

During meiosis, germ cell and stage-specific components impose additional layers of regulation on the core cell cycle machinery to set up an extended G2 period termed meiotic prophase. In Drosophila males, meiotic prophase lasts 3.5 days, during which spermatocytes turn up expression of over 3000 genes and grow 25-fold in volume. Previous work showed that the core cell cycle regulator Cyclin B (CycB) is subject to translational repression in immature Drosophila spermatocytes, mediated by the RNA-binding protein Rbp4 and its partner Fest. Here we show that another spermatocyte-specific protein, Lut, is required for translational repression of cycB in an 8-hour window just before spermatocytes are fully mature. In males mutant for rbp4 or lut , spermatocytes enter and exit the meiotic divisions 6-8 hours earlier than in wild-type. In addition, we show that spermatocyte-specific isoforms of Syncrip (Syp) are required for expression of CycB protein and normal entry into the meiotic divisions. Both Lut and Syp interact with Fest in an RNA-independent manner. Thus a complex of spermatocyte-specific regulators choreograph the timing of expression of CycB protein during male meiotic prophase. SUMMARY STATEMENT: Expression of a conserved cell cycle component, Cyclin B, is regulated by multiple mechanisms in the Drosophila male germline to dictate the correct timing of meiotic division.