A Tudor Domain Protein SPINDLIN1 Interacts with the mRNA-Binding Protein SERBP1 and Is Involved in Mouse Oocyte Meiotic Resumption

Ting Gang Chew,Anne Peaston,Chanchao Lorthongpanich,Barbara B Knowles,Ai Khim Lim,Davor Solter,Qing-Yuan Sun

doi:10.1371/journal.pone.0069764

Abstract

Mammalian oocytes are arrested at prophase I of meiosis, and resume meiosis prior to ovulation. Coordination of meiotic arrest and resumption is partly dependent on the post-transcriptional regulation of maternal transcripts. Here, we report that, SPINDLIN1 (SPIN1), a maternal protein containing Tudor-like domains, interacts with a known mRNA-binding protein SERBP1, and is involved in regulating maternal transcripts to control meiotic resumption. Mouse oocytes deficient for Spin1 undergo normal folliculogenesis, but are defective in resuming meiosis. SPIN1, via its Tudor-like domain, forms a ribonucleoprotein complex with SERBP1, and regulating mRNA stability and/or translation. The mRNA for the cAMP-degrading enzyme, PDE3A, is reduced in Spin1 mutant oocytes, possibly contributing to meiotic arrest. Our study demonstrates that Spin1 regulates maternal transcripts post-transcriptionally and is involved in meiotic resumption.

Highlights

During fetal development in mammals, the female germ cell enters meiosis and arrests at meiotic prophase I with a distinctive germinal vesicle (GV) in the cell center
Characterization of Spin1 genetrap homozygous fetal gonads at E18.5 shows that Spin1 mRNA and proteins are barely detectable in these tissues, indicating that the Spin1 genetrap homozygote is a null allele for Spin1 function (Figure S1C and D)
Through characterizing a mouse mutant defective in Spin1 and identifying its protein interacting partners, we have established that SPIN1 forms an RNP complex with the mRNA-binding protein SERBP1 and is involved in the resumption of meiosis in mammalian oocytes

Summary

Introduction

During fetal development in mammals, the female germ cell enters meiosis and arrests at meiotic prophase I with a distinctive germinal vesicle (GV) in the cell center. After a long period of meiotic arrest and oocyte growth, the fully grown oocyte resumes meiosis upon the stimulation of hormones during puberty [1]. The resumption and completion of meiosis are highly dependent on maternal mRNAs and proteins stored during oocyte growth [4,5,6,7]. Maternal mRNAs form ribonucleoprotein (RNP) complexes with RNA-binding proteins, which stabilize the maternal mRNAs and the mRNAs are translated into proteins in a just-in-time fashion [8,9]. The mRNAs of several cell cycle regulatory proteins are stabilized and timely translated during the transition of meiotic arrest to meiotic resumption [6,7,10]

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