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Cell Biosci. 2018 Oct 19;8:54. doi: 10.1186/s13578-018-0251-1. eCollection 2018.

A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis.

Mak W1,2, Xia J3, Cheng EC3, Lowther K4, Lin H3,5,1,6,7.

Author information

1
3Division of Reproductive Endocrinology and Infertility, Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale University School of Medicine, New Haven, CT 06519 USA.
2
Women's Health Department, Dell Medical School, Medical Park Tower, 1301 W. 38th Street, Suite 705, Austin, TX 78705 USA.
3
1Yale Stem Cell Center, Yale University School of Medicine, 10 Amistad Street, New Haven, CT 06519 USA.
4
6University of Connecticut Health Center, Farmington, CT 06030 USA.
5
2Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06519 USA.
6
4Department of Genetics, Yale University School of Medicine, New Haven, CT 06519 USA.
7
5SIAIS and School of Life Science and Technology, Shanghai Tech University, Shanghai, China.

Abstract

Background:

RNA binding proteins play a pivotal role during the oocyte-to-embryo transition and maternal phase of embryogenesis in invertebrates, but their function in these processes in mammalian systems remain largely understudied.

Results:

Here we report that a member of the Pumilio/FBF family of RNA binding proteins in mice, Pumilio 1 (Pum1), is a maternal effect gene. The absence of maternal PUM1 in the oocyte does not affect meiotic maturation but leads to abnormal preimplantation development. Furthermore, genome-wide transcriptome analysis of oocytes and embryos revealed that there is a concomitant perturbation of the mRNA milieu. Of note, putative PUM1 mRNA targets were equally perturbed as non-direct targets, which indicates that PUM1 regulates the stability of maternal mRNAs both directly and indirectly. We show Cdk1 mRNA, a known PUM1 target essential for meiosis and preimplantation development, is not degraded appropriately during meiosis, leading to an increase in CDK1 protein in mature oocytes, which indicates that PUM1 post-transcriptionally regulates Cdk1 mRNA; this could partially explain the observed abnormal preimplantation development. Furthermore, our results show that maternal and zygotic PUM1 are required for postnatal survival.

Conclusions:

These findings indicate that PUM1 is essential in the process of cytoplasmic maturation and developmental competence of the oocyte. These results reveal an important function of maternal PUM1 as a post-transcriptional regulator during mammalian embryogenesis.

KEYWORDS:

Oocyte maturation; Post-transcriptional regulation; Preimplantation embryo

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