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

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

PROVIDER: PRJNA899845 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	SRR22245800.fastq.gz	Fastqsanger.gz
	SRR22245900.fastq.gz	Fastqsanger.gz
	SRR22245801_1.fastq.gz	Fastqsanger.gz
	SRR22245801_2.fastq.gz	Fastqsanger.gz
	SRR22245901.fastq.gz	Fastqsanger.gz

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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.

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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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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.

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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 mammalian reproduction remains poorly understood outside of mice. Here, we describe the expression profiles, subcellular localization, and knockout-associated reproductive defects for all four PIWIs in golden hamsters. In female golden hamsters, PIWIL1 and PIWIL3 are highly expressed throughout oogenesis and early embryogenesis, while knockout of PIWIL1 leads to sterility, and PIWIL3 deficiency results in subfertility with lagging zygotic development. PIWIL1 can partially compensate for TE silencing in PIWIL3 knockout females, but not vice versa. PIWIL1 and PIWIL4 are the predominant PIWIs expressed in adult and postnatal testes, respectively, while PIWIL2 is present at both stages. Loss of any PIWI expressed in testes leads to sterility and severe but distinct spermatogenesis disorders. These findings illustrate the non-redundant regulatory functions of PIWI-piRNAs in gametogenesis and early embryogenesis in golden hamsters, facilitating study of their role in human fertility.

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Project description:PIWI-associated RNAs (piRNAs) support germline by suppressing retrotransposons and genes. In mice, piRNAs are essential for spermatogenesis but not oogenesis. To test how this applies to other mammals, we deleted Mov10l1 helicase in golden hamsters whose piRNA pathway configuration is closer to other mammals than that of mice. Mov10l1–/– male hamsters showed impaired establishment of spermatogonia accompanied by transcriptome dysregulation and surge of MYSERV retrotransposon expression. The rare viable spermatogenic cells showed meiotic failure phenotype like Mov10l1–/– mice. Female Mov10l1–/–hamsters were sterile due to post-meiotic loss of developmental competence in zygotes. Unique phenotypes of Mov10l1–/– hamsters demonstrate adaptive nature of piRNA-mediated control of genes and retrotransposons, which enables confronting emerging genomic threats or acquiring new physiological roles.

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