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Integrated small and long RNA sequencing in single oocytes reveals piRNA-mediated transposon repression during human oogenesis

ABSTRACT: In this study, we simultaneously profiled small and long RNA transcriptomes in individual human oocytes across four developmental stages. piRNAs, especially PIWIL3-associated short piRNAs (short-piRNAs), are the predominant small non-coding RNAs during human oogenesis. A marked increase in short-piRNAs after the primordial follicle stage coincided with a global downregulation of TE expression, particularly LINE-1 (L1) and endogenous retroviruses (ERVs). On the other hand, PIWIL1- and PIWIL2-associated long piRNAs (long-piRNAs) were correlated with the silencing of certain specific ERV subfamilies. Genomic-context analyses revealed that highly productive piRNA clusters have evolved asymmetric antisense insertion bias toward L1 and ERVs, contributing to TE families-specific regulation.

ORGANISM(S): Homo sapiens

PROVIDER: GSE296363 | GEO | 2026/02/06

REPOSITORIES: GEO

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Piwi proteins and piRNAs in mammalian oocytes and early embryos

Project description:Germ cells of most animals critically depend on piRNAs and Piwi proteins. Surprisingly, piRNAs in mouse oocytes are relatively rare and dispensable. We present compelling evidence for strong Piwi-piRNA expression in oocytes of other mammals. Human fetal oocytes express PIWIL2 and transposon-enriched piRNAs. Oocytes in adult human ovary express PIWIL1 and PIWIL2, while those in bovine ovary just express PIWIL1. In human, macaque and bovine ovaries we find piRNAs that resemble testis-borne pachytene piRNAs. Isolated bovine follicular oocytes were shown to contain abundant, relatively short piRNAs that preferentially target transposable elements. Using label-free quantitative proteome analysis we show that these maturing oocytes strongly and specifically express the thus-far uncharacterized PIWIL3 protein, alongside other known piRNA-pathway components. In bovine early embryos these piRNAs are still abundant, revealing a potential impact of piRNAs on mammalian embryogenesis. Our results reveal unexpected, highly dynamic piRNA pathways in mammalian oocytes and early embryos. Analyses of multiple small RNA libraries obtained from fetal/adult oocytes, cumulus cells, ovary, testis and 2-4 cell stage ivf embryos of multiple mammalian species.

2015-03-27 | E-GEOD-64942 | biostudies-arrayexpress

Piwi proteins and piRNAs in mammalian oocytes and early embryos

2015-03-27 | GSE64942 | GEO

The non-redundant functions of PIWI family proteins in gametogenesis in golden hamsters

Project description:The piRNA pathway is essential for female fertility in golden hamsters and likely humans, but not in mice. However, the role of individual PIWIs in reproduction remains poorly understood outside of mice. Here, using golden hamsters, we establish dynamic expression profiles and subcellular localization for all four PIWIs and characterize their associated reproductive defects in knockout mutants. In female golden hamsters, PIWIL1 and PIWIL3 are highly expressed throughout oogenesis and early embryogenesis, while PIWIL1 knockout leads to sterility, and PIWIL3 deficiency results in subfertility with lagging zygotic development. PIWIL1 can partially compensate for TE silencing and transcriptional regulation in PIWIL3 knockout females, but not vice versa. PIWIL1 and PIWIL4 are the predominant PIWIs expressed in adult or postnatal testes, respectively, while PIWIL2 is present in both stages. Notably, in golden hamsters, none of the differences were found between pre-pachytene and pachytene piRNAs characteristic of mice. Loss of any PIWI expressed in testes leads to sterility and severe but distinct spermatogenesis disorders, which are markedly less severe in mice. These findings expand our understanding of the non-redundant PIWI-piRNA regulatory functions in gametogenesis and early embryogenesis in golden hamster, increasing the value of this model for studying human fertility.

2023-07-13 | GSE217621 | GEO

piRNA pathway is essential for generating functional oocytes in golden hamster

Project description:Piwi-interacting RNAs (piRNAs) are small RNAs predominantly expressed in germ cells that function in gametogenesis in various species. Notably, PIWI-deficient female mice are fertile and mouse oocytes express a panel of small RNAs that do not appear widely representative of mammals. Thus, the function of piRNAs in mammalian oogenesis remains largely elusive. Here, we generated PIWIL1- and MOV10L1-deficient golden hamsters and found that all female and male mutants were sterile, with severe defects in embryogenesis and spermatogenesis, respectively. PIWIL1-deficient oocytes displayed aberrant transposon accumulation and broad transcriptomic dysregulation, and maternal PIWIL1-deficient embryos had impaired zygotic genome activation (ZGA). Moreover, our results support that PIWIL1-piRNAs exert a non-redundant function in silencing endogenous retroviruses (ERVs) in oocytes. Together, our findings demonstrate that piRNAs are indispensable for generating functional germ cells in golden hamsters and show the informative value of this model species for functional and mechanistic investigations of piRNAs in gametogenesis, especially those related to female infertility.

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PIWIL3 forms a complex with TDRKH in mammalian oocytes

Project description:PIWIs are crucial guardians of genome integrity, particularly in germ cells. While mammalian PIWIs have been primarily studied in mouse and rat, a homologue for the human PIWIL3 geneis absent in the Muridae family, and hence the unique function of PIWIL3 in germ cells cannot be effectively modeled by mouse knockouts. Herein, we investigated the expression,distribution and interaction of PIWIL3 in bovine oocytes. We localized PIWIL3 to mitochondria, and demonstrated that PIWIL3 expression is stringently controlled both spatially and temporally before and after fertilization. Moreover, we identified PIWIL3 in a mitochondrial-recruited three-membered complex with TDRKH and PNLDC1, and demonstrated by mutagenesis that PIWIL3 N-terminal arginine modifications are required for complex assembly. Finally we sequenced the piRNAs bound to PIWIL3-TDRKH-PNLDC1 and report here that about 50% of these piRNAs map to transposable elements, recapitulating the important role of PIWIL3 in maintaining genome integrity in mammalian oocytes.

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Project description:We found piRNAs with different lengths represented the predominant small RNA species in oocytes from the 12 explored species, except mouse. We found endo-siRNAs resulted from the truncated Dicer isoform were mouse-specific, and os-piRNAs associating with PIWIL3 in human oocytes are widespread in mammals and are typically with low levels of the 2’-3’-O-methylation. The sequences of many highly expressed piRNA clusters are fast-evolving compared with their syntenic genomic locations, and the TE families distributing in the conserved piRNA clusters are various between species.

2024-03-06 | GSE200470 | GEO

Divergent composition and transposon-silencing activity of small RNAs in mammalian oocytes II

2024-03-06 | GSE256514 | GEO

The piRNAs bounding to Piwil2 in the CA1 region of the transient Global Cerebral Ischemia rats hippocampus

Project description:Purpose：To identify piRNAs bound to Piwil2 in Sham,transient Global Cerebral Ischemia(tGCI) and transient Global Cerebral Ischemia(tGCI) with Hypoxic Postconditioning (HPC). Methods: Samples from CA1 subregion were lysed in 500 μl lysis buffer and centrifuged. After centrifugation, supernatant was incubated with monoclonal mouse antibody against Piwil2 (Santa Cruz, California, CA, USA), preincubated with Protein A/G Agarose. The beads were washed twice with lysis buffer. After quality check by Western blot, the RNA was extracted from the magnetic beads using Trizol reagent (Invitrogen). Then, the immunoprecipitated RNA was analyzed with piRNAs sequencing. Results: After tGCI, a total of 423 piRNAs interacted with Piwil2 in CA1 was upregulated after 26 h of reperfusion. Of the 423 piRNAs, 317 were significantly upregulated by more than 1.5-fold. Of the 317 piRNAs, 258 showed ≥2-fold change. Comparison between tGCI and HPC groups revealed that 401 piRNAs interacted with Piwil2 in CA1 were significantly downregulated after HPC, whereas only 7 piRNAs were found to be altered in all 3 groups studied (≥1.5-fold change). Conclusions: In our study, we identified a cohort of piRNAs in CA1 of rats. We demonstrated directly contrast changes of piRNAs interacted with Piwil2 in CA1 after tGCI, as compared to those in HPC rats. The results of the prediction showed that DNMT3A may be a potential common target of the 7 differentially expressed piRNAs interacted with Piwil2. Therefore, we focused on the expression of DNMT3A in CA1 after tGCI with or without HPC.

2023-01-18 | GSE163299 | GEO

PIWIL2 downregulation in colon cancer promotes transposon activity and pro-tumorigenic phenotypes

Project description:Reactivation of transposable elements (TEs) in somatic tissues, particularly of LINE-1, is associated with disease by causing gene mutations and DNA damage. Previous work has shown that the PIWI pathway is crucial for TE suppression in the germline. However, the status and function of this pathway is not well characterized in differentiated somatic cells and there is lack of consensus on the role of the pathway in somatic tumorigenesis. To shed light on this conundrum, we examined the PIWI pathway in colon cancer through combining bioinformatic analyses and cell-based assays. Shifted Weighted Annotation Network (SWAN) analysis revealed that the pathway experiences significant allelic losses in colon cancer and that PIWIL2, the main catalytic component of the pathway responsible for TE silencing, experiences the highest percent deletions. PIWIL2 is downregulated in colon tumors of advanced stage, nodal metastasis, and in certain subtypes, correlating with poor survival, while it is also downregulated in ulcerative colitis, an inflammatory bowel disease that predisposes to colon cancer. PIWIL2 depletion in colon epithelial Caco2 cells leads to increased anchorage-independent growth, loss of transposon-targeting - non-canonical - piRNAs, increased LINE-1 levels and activity, and in DNA damage, altogether highlighting a tumor-suppressing role of PIWIL2 in the colon.

2025-07-31 | GSE303118 | GEO

Production of functional oocytes requires maternally expressed PIWI genes and piRNAs in golden hamsters

Project description:Many animals have a conserved adaptive genome defense system known as the Piwi-interacting RNA (piRNA) pathway which is essential for germ cell development and function. Disruption of individual mouse Piwi genes results in male but not female sterility, leading to the assumption that PIWI genes do not play a role in mammalian oocytes. Contrary to this, PIWIL1- and PIWIL3-defective golden hamsters we have produced show defects in production of functional oocytes. Mechanisms involved, however, vary between the two PIWI genes; lack of PIWIL1 has a strong impact on gene expression including hamster-specific young transposon de-silencing, while PIWIL3 deficiency has little impact on gene expression in oocytes, although DNA methylation of chromosomes was reduced to some extent. Our findings serve as the foundation for developing useful models to study the piRNA pathway in mammalian oocytes including humans, which cannot be possible with mice.

2021-07-02 | GSE164356 | GEO

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