A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis
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 fa...
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| Format: | Article |
| Language: | English |
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BMC
2018-10-01
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| Series: | Cell & Bioscience |
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| Online Access: | http://link.springer.com/article/10.1186/s13578-018-0251-1 |
| _version_ | 1818291435353407488 |
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| author | Winifred Mak Jing Xia Ee-Chun Cheng Katie Lowther Haifan Lin |
| author_facet | Winifred Mak Jing Xia Ee-Chun Cheng Katie Lowther Haifan Lin |
| author_sort | Winifred Mak |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-13T02:44:01Z |
| format | Article |
| id | doaj.art-3bf0759c96c748f4ba5704c1cd4d0c7d |
| institution | Directory Open Access Journal |
| issn | 2045-3701 |
| language | English |
| last_indexed | 2024-12-13T02:44:01Z |
| publishDate | 2018-10-01 |
| publisher | BMC |
| record_format | Article |
| series | Cell & Bioscience |
| spelling | doaj.art-3bf0759c96c748f4ba5704c1cd4d0c7d2022-12-22T00:02:13ZengBMCCell & Bioscience2045-37012018-10-018111710.1186/s13578-018-0251-1A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesisWinifred Mak0Jing Xia1Ee-Chun Cheng2Katie Lowther3Haifan Lin4Division of Reproductive Endocrinology and Infertility, Department of Obstetrics, Gynecology, and Reproductive Sciences, Yale University School of MedicineYale Stem Cell Center, Yale University School of MedicineYale Stem Cell Center, Yale University School of MedicineUniversity of Connecticut Health CenterYale Stem Cell Center, Yale University School of MedicineAbstract 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.http://link.springer.com/article/10.1186/s13578-018-0251-1Post-transcriptional regulationOocyte maturationPreimplantation embryo |
| spellingShingle | Winifred Mak Jing Xia Ee-Chun Cheng Katie Lowther Haifan Lin A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis Cell & Bioscience Post-transcriptional regulation Oocyte maturation Preimplantation embryo |
| title | A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis |
| title_full | A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis |
| title_fullStr | A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis |
| title_full_unstemmed | A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis |
| title_short | A role of Pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis |
| title_sort | role of pumilio 1 in mammalian oocyte maturation and maternal phase of embryogenesis |
| topic | Post-transcriptional regulation Oocyte maturation Preimplantation embryo |
| url | http://link.springer.com/article/10.1186/s13578-018-0251-1 |
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