Cyclin B3 (CCNB3) plays a critical regulatory role in mammalian meiosis. Studies in mice have demonstrated that CCNB3 interacts with CDK1 to modulate the activity of MPF, thereby driving meiotic progression. However, the functional mechanisms of CCNB3 in porcine oocytes remain unclear. In this study, we reveal for the first time that knockdown of CCNB3 in porcine oocytes induces meiotic arrest at metaphase I, accompanied by impaired degradation of cyclin B1 and securin. Further investigation identifies that the antisense long non-coding RNA CCNB3-AS forms a double-stranded RNA (dsRNA) structure with the CCNB3 mRNA, significantly enhancing its stability by resisting PAT1 homolog 1 (PATL1)-mediated degradation. Mechanistically, CCNB3-AS interacts with the scaffold protein Vimentin (VIM). Structural analysis reveals that VIM binds to the PAT1 domain of PATL1 and is capable of influencing the ability of CNOT7, the core subunit of the CCR4-NOT complex, to bind to PATL1, ultimately maintaining stable CCNB3 mRNA expression. Our study elucidates the molecular mechanism by which the CCNB3-AS/CCNB3 dsRNA duplex cooperates with VIM and PATL1 to collectively regulate meiosis in porcine oocytes. Furthermore, we reveal the non-canonical role of VIM in mRNA degradation, providing new theoretical support for understanding the mechanisms underlying porcine oocyte meiosis.
Zhu et al. (Mon,) studied this question.