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Positive Feedback Stimulation of Ccnb1 and Mos mRNA Translation by MAPK Cascade During Mouse Oocyte Maturation
Lan-Rui Cao1, Jun-Chao Jiang1, Heng-Yu Fan1
1Life Sciences Institute, Zhejiang University, Hangzhou, China.
Abstract:
In mammalian species, both the maturation promoting factor (MPF) and the mitogen-activated protein kinase (MAPK) cascade play critical roles in modulating oocyte meiotic cell-cycle progression. MPF is a critical heterodimer composed of CDK1 and cyclin B1. Activation of MPF and ERK1/2 requires the activation of maternal Ccnb1 and Mos mRNAs translation, respectively. The phosphorylation and degradation of CPEB1 that triggered by ERK1/2 is a principal mechanism of activating maternal mRNA translation. However, the interplay of these two key kinases in mediating mammalian translational activation of cytoplasmic mRNAs during oocyte maturation is unclear. We prove evidence that the translational activation of Ccnb1 transcripts containing a long 3'-UTR during meiotic resumption works in an ERK1/2-dependent way. A low level of ERK1/2 activation was detected prior to meiotic resumption. Precocious activation of MAPK signaling in germinal vesicle stage oocytes promotes the translation of Ccnb1 mRNA and meiotic maturation. Inhibition or precocious activation of CDK1 activity has an appreciable effect on the translation of Ccnb1 mRNA, suggesting that both kinases are required for Ccnb1 mRNA translational activation. CDK1 triggers phosphorylation, but not degradation, of CPEB1 in oocytes; the degradation of CPEB1 was only triggered by ERK1/2. Moreover, the translational activation of Mos mRNA is regulated by ERK1/2 and cytoplasmic polyadenylation elements too. Taken together, the cooperation and positive feedback activation of ERK1/2 and CDK1 lead to the fine-tuning of mRNA translation and cell-cycle progression during mouse oocyte maturation.
Insights
The study reveals that both ERK1/2 and CDK1 kinases cooperate to control maternal mRNA translation, fine-tuning cell-cycle progression during mouse oocyte maturation through a positive feedback loop.
Area of Science:
- Cell Biology
- Molecular Biology
- Developmental Biology
Background:
- Oocyte maturation involves complex cell-cycle regulation controlled by key signaling pathways.
- Maturation promoting factor (MPF) and mitogen-activated protein kinase (MAPK) cascades are crucial for meiotic progression.
- Understanding the interplay of these kinases in translational control of maternal mRNAs is essential.
Purpose of the Study:
- To elucidate the interplay between ERK1/2 and CDK1 in regulating maternal mRNA translation during mammalian oocyte maturation.
- To investigate the role of ERK1/2 and CDK1 in the translational activation of specific mRNAs like Ccnb1 and Mos.
- To determine the precise mechanisms by which these kinases influence cytoplasmic mRNA translation and cell-cycle progression.
Main Methods:
- Investigated the translational activation of Ccnb1 mRNA during meiotic resumption.
- Examined the effects of inhibiting or precociously activating CDK1 activity on Ccnb1 mRNA translation.
- Analyzed the phosphorylation and degradation of CPEB1 by ERK1/2 and CDK1.
Main Results:
- Translational activation of Ccnb1 mRNA is ERK1/2-dependent during meiotic resumption.
- Both ERK1/2 and CDK1 are required for Ccnb1 mRNA translational activation.
- ERK1/2 triggers CPEB1 degradation, while CDK1 triggers its phosphorylation; ERK1/2 is solely responsible for degradation.
- ERK1/2 and cytoplasmic polyadenylation elements regulate Mos mRNA translation.
Conclusions:
- Cooperation and positive feedback between ERK1/2 and CDK1 fine-tune mRNA translation and cell-cycle progression in mouse oocytes.
- This intricate kinase interplay is critical for successful oocyte maturation.
- The findings provide new insights into the molecular mechanisms governing meiotic cell-cycle control.
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