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Pumilio1 phosphorylation precedes translational activation of its target mRNA in zebrafish oocytes

Published online by Cambridge University Press:  05 October 2018

Atsushi Saitoh ,
Yuki Takada ,
Mayu Horie  and
Tomoya Kotani Open the ORCID record for Tomoya Kotani [Opens in a new window]
Atsushi Saitoh
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan
Yuki Takada
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan
Mayu Horie
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan
Tomoya Kotani*
Affiliation:
Biosystems Science Course, Graduate School of Life Science, Hokkaido University, Sapporo 060-0810, Japan Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan.
*
*Author for correspondence: T Kotani. Department of Biological Sciences, Faculty of Science, Hokkaido University, North 10 West 8, Sapporo, Hokkaido 060-0810, Japan. Tel/Fax: +81 11 7064455. E-mail: [email protected]
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Summary

Translational regulation of mRNAs is crucial for promoting various cellular and developmental processes. Pumilio1 (Pum1) has been shown to play key roles in translational regulation of target mRNAs in many systems of diverse organisms. In zebrafish immature oocytes, Pum1 was shown to bind to cyclin B1 mRNA and promote the formation of cyclin B1 RNA granules. This Pum1-mediated RNA granule formation seemed critical to determine the timing of translational activation of cyclin B1 mRNA during oocyte maturation, leading to activation of maturation/M-phase-promoting factor (MPF) at the appropriate timing. Despite its fundamental importance, the mechanisms of translational regulation by Pum1 remain elusive. In this study, we examined the phosphorylation of Pum1 as a first step to understand the mechanisms of Pum1-mediated translation. SDS-PAGE analyses and phosphatase treatments showed that Pum1 was phosphorylated at multiple sites during oocyte maturation. This phosphorylation began in an early period after induction of oocyte maturation, which preceded the polyadenylation of cyclin B1 mRNA. Interestingly, depolymerization of actin filaments in immature oocytes caused phosphorylation of Pum1, disassembly of cyclin B1 RNA granules, and polyadenylation of cyclin B1 mRNA but not translational activation of the mRNA. Overexpression of the Pum1 N-terminus prevented the phosphorylation of Pum1, disassembly of cyclin B1 RNA granules, and translational activation of the mRNA even after induction of oocyte maturation. These results suggest that Pum1 phosphorylation in the early period of oocyte maturation is one of the key processes for promoting the disassembly of cyclin B1 RNA granules and translational activation of target mRNA.

Keywords

Cytoplasmic polyadenylationOocyte maturationRNA granuleTranslationVertebrate
Type
Research Article
Information
Zygote , Volume 26 , Issue 5 , October 2018 , pp. 372 - 380
Copyright
© Cambridge University Press 2018 

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