Journal
BIOLOGY OF REPRODUCTION
Volume 82, Issue 1, Pages 123-131Publisher
OXFORD UNIV PRESS INC
DOI: 10.1095/biolreprod.109.076588
Keywords
3 '-untranslated region; gamete biology; gametogenesis; gene regulation; meiotic maturation; oocyte development; oogenesis; ovum; proteasome; protein degradation; stem-loop-binding protein; translational control
Categories
Funding
- Canadian Institutes for Health Research
- Program in Oocyte Health
- Fonds de Recherche en Sante du Quebec
- Royal Victoria Hospital Foundation
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Developmentally regulated translation plays a key role in controlling gene expression during oogenesis. In particular, numerous mRNA species are translationally repressed in growing oocytes and become translationally activated during meiotic maturation. While many studies have focused on a U-rich sequence, termed the cytoplasmic polyadenylation element (CPE), located in the 3'-untranslated region (UTR) and the CPE-binding protein (CPEB) 1, multiple mechanisms likely contribute to translational control in oocytes. The stem-loop-binding protein (SLBP) is expressed in growing oocytes, where it is required for the accumulation of nonpolyadenylated histone mRNAs, and then accumulates substantially during meiotic maturation. We report that, in immature oocytes, Slbp mRNA carries a short poly( A) tail, and is weakly translated, and that a CPE-like sequence in the 3'-UTR is required to maintain this low activity. During maturation, Slbp mRNA becomes polyadenylated and translationally activated. Unexpectedly, proteasomal activity is required both to initiate and to sustain translational activation. This proteasomal activity is not required for the polyadenylation of Slbp mRNA during early maturation; however, it is required for a subsequent deadenylation of the mRNA that occurs during late maturation. Moreover, although CPEB1 is degraded during maturation, inhibiting its degradation by blocking mitogen-activated protein kinase 1/3 activity does not prevent the accumulation of SLBP, indicating that CPEB1 is not the protein whose degradation is required for translational activation of Slbp mRNA. These results identify a new role for proteasomal activity in initiating and sustaining translational activation during meiotic maturation.
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