A role for Drosophila Cyclin J in oogenesis revealed by genetic interactions with the piRNA pathway

Abstract

Cyclin J (CycJ) is a poorly characterized member of the Cyclin superfamily of cyclin-dependent kinase regulators, many of which regulate the cell cycle or transcription. Although CycJ is conserved in metazoans its cellular function has not been identified and no mutant defects have been described. In Drosophila, CycJ transcript is present primarily in ovaries and very early embryos, suggesting a role in one or both of these tissues. The CycJ gene (CycJ) lies immediately downstream of armitage (armi), a gene involved in the Piwi-associated RNA (piRNA) pathways that are required for silencing transposons in the germline and adjacent somatic cells. Mutations in armi result in oogenesis defects but a role for CycJ in oogenesis has not been defined. Here we assessed oogenesis in CycJ mutants in the presence or absence of mutations in armi or other piRNA pathway genes. CycJ null ovaries appeared normal, indicating that CycJ is not essential for oogenesis under normal conditions. In contrast, armi null ovaries produced only two egg chambers per ovariole and the eggs had severe axis specification defects, as observed previously for armi and other piRNA pathway mutants. Surprisingly, the CycJ armi double mutant failed to produce any mature eggs. The double null ovaries generally had only one egg chamber per ovariole and the egg chambers frequently contained an overabundance of differentiated germline cells. Production of these compound egg chambers could be suppressed with CycJ transgenes but not with mutations in the checkpoint gene mnk, which suppress oogenesis defects in armi mutants. The CycJ null showed similar genetic interactions with the germline and somatic piRNA pathway gene piwi, and to a lesser extent with aubergine (aub), a member of the germline-specific piRNA pathway. The strong genetic interactions between CycJ and piRNA pathway genes reveal a role for CycJ in early oogenesis. Our results suggest that CycJ is required to regulate egg chamber production or maturation when piRNA pathways are compromised.

Genome-Wide Identification, Expression Profiling, and Characterization of Cyclin-like Genes Reveal Their Role in the Fertility of the Diamondback Moth

“…High expressions of cyclin genes in reproductive tissues indicate that cyclin genes may have some distinct role in reproduction beyond the growth and development. Previous studies in some model organisms show that cyclin genes play specific roles in ovary development and oogenesis [ 67 , 68 ]. In D. melanogaster , cyclin B and cyclin B3 are involved in female and male fertility [ 15 ], while cyclin J and cyclin G are involved in egg chamber maturation and wing development [ 16 , 68 ].…”

Enterocyte Purge and Rapid Recovery Is a Resilience Reaction of the Gut Epithelium to Pore-Forming Toxin Attack

“…and N. Nehme, unpublished data). It encodes a highly conserved cyclin of unknown function in somatic cells (Althoff et al, 2009;Atikukke et al, 2014). As shown in Figure 6A and Figure S4A, both null mutant flies and flies in which CycJ expression was knocked down by RNAi in enterocytes underwent the thinning of the intestinal epithelium yet failed to recover from hemolysin attack.…”

Co-expression Patterns Explain how a Basic Transcriptional Role for MYC Modulates Wnt and MAPK Pathways in Colon and Lung Adenocarcinomas

“…CCNJ, CCNO:Cdk2, CCNG1:Cdk4/5/6, CCNI:Cdk5 CCNJ knockdown in Drosophila leads to defects in chromosome segregation and progression through mitosis in early embryonic division cycles [34,35]. Complete complexes necessary for origin licensing, firing, and DNA synthesis were not coexpressed fully with CCNJ, in agreement with a role for CCNJ downstream of most of these functions.…”