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Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells.

ABSTRACT: Transposable elements (TEs), whose propagation can result in severe damage to the host genome, are silenced in the animal gonad by Piwi-interacting RNAs (piRNAs). piRNAs produced in the ovaries are deposited in the embryonic germline and initiate TE repression in the germline progeny. Whether the maternally transmitted piRNAs play a role in the silencing of somatic TEs is however unknown. Here we show that maternally transmitted piRNAs from the tirant retrotransposon in Drosophila are required for the somatic silencing of the TE and correlate with an increase in histone H3K9 trimethylation an active tirant copy.

SUBMITTER: Akkouche A

PROVIDER: S-EPMC3642378 | biostudies-literature | 2013 May

REPOSITORIES: biostudies-literature

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Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells.

Akkouche Abdou A Grentzinger Thomas T Fablet Marie M Armenise Claudia C Burlet Nelly N Braman Virginie V Chambeyron Séverine S Vieira Cristina C

EMBO reports 20130405 5

Transposable elements (TEs), whose propagation can result in severe damage to the host genome, are silenced in the animal gonad by Piwi-interacting RNAs (piRNAs). piRNAs produced in the ovaries are deposited in the embryonic germline and initiate TE repression in the germline progeny. Whether the maternally transmitted piRNAs play a role in the silencing of somatic TEs is however unknown. Here we show that maternally transmitted piRNAs from the tirant retrotransposon in Drosophila are required f ...[more]

PMID: 23559065

Similar Datasets

Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells

Project description:Transposable elements (TEs), whose propagation can result in severe damage to the host genome, are silenced in the animal gonad by Piwi-interacting RNAs (piRNAs). piRNAs produced in the ovaries are deposited in the embryonic germline and initiate TE repression in the germline progeny. Whether the maternally transmitted piRNAs play a role in the silencing of somatic TEs is, however, unknown. Here we show that maternally transmitted piRNAs from the tirant retrotransposon in Drosophila are required for the somatic silencing of the TE and correlate with an increase in histone H3K9 trimethylation an active tirant copy. Comparison of tirant piRNAs in two Drosophila simulans natural populations.

2013-04-09 | E-GEOD-40592 | biostudies-arrayexpress

Maternally deposited germline piRNAs silence the tirant retrotransposon in somatic cells

2013-04-09 | GSE40592 | GEO

Maternally inherited piRNAs silence transposons during Drosophila embryogenesis

Project description:The piRNA pathway controls transposon expression in animal germ cells, thereby ensuring genome stability over generations. piRNAs are maternally deposited and required for proper transposon silencing in adult offspring. However, a long-standing question in the field is the precise function of maternally deposited piRNAs and its associated factors during embryogenesis. Here, we probe the spatio-temporal expression patterns of several piRNA pathway components during early stages of development. Amongst those, factors required for transcriptional gene silencing (TGS) showed ubiquitous abundance in somatic and pole cells throughout the first half of embryogenesis. We further analysed the transcriptomes of various embryo stages and correlated these with the presence of selected chromatin marks. We found that a number of transposon families show bursts of transcription during early embryonic stages. Transposons heavily targeted by maternally deposited piRNAs accumulated repressive chromatin marks following their spike in expression. Furthermore, depletion of maternally deposited Piwi protein in early embryos resulted in increased expression of transposons targeted by inherited piRNAs and was accompanied by a strong loss of repressive chromatin marks at coding sequences. Overall, our data suggests a pivotal role for the piRNA pathway in transposon defence during Drosophila embryogenesis in somatic cells.

2021-07-26 | PXD022409 | Pride

Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies.

Project description:Piwi-interacting RNAs (piRNAs) silence transposons in animal germ cells. piRNAs are thought to derive from long transcripts spanning transposon-rich genomic loci and to direct an autoamplification loop in which an antisense piRNA, bound to Aubergine or Piwi protein, triggers production of a sense piRNA bound to the PIWI protein Argonaute3 (Ago3). In turn, the new piRNA is envisioned to produce a second antisense piRNA. Here, we describe strong loss-of-function mutations in ago3, allowing a direct genetic test of this model. We find that Ago3 acts to amplify piRNA pools and to enforce on them an antisense bias, increasing the number of piRNAs that can act to silence transposons. We also detect a second, Ago3-independent piRNA pathway centered on Piwi. Transposons targeted by this second pathway often reside in the flamenco locus, which is expressed in somatic ovarian follicle cells, suggesting a role for piRNAs beyond the germline.

| S-EPMC2768572 | biostudies-literature

Germline piRNAs counteract endogenous retrovirus invasion from somatic cells

Project description:In metazoan gonads, transposable elements (TEs) mobilization is limited by PIWI-interacting RNAs (piRNAs). These small RNAs originate from specific source loci, the piRNA clusters. piRNAs are known to silence TEs in the cells where they are produced. Endogenous retroviruses (ERVs), a subclass of TEs, pose a particular threat because they are capable of transiting from cell to cell. In this study, we reveal that piRNAs produced locally in germ cells counteract invasion by ERVs arriving from adjacent somatic cells. We reactivated the Drosophila ERVZAMin somatic gonadal cells by deleting, using CRISPR-Cas9 genome editing, its single copy in the somaticflamencopiRNA cluster, while keeping the piRNA pathway fully functional. Upon reactivation,ZAMinvaded the oocytes, resulting in transposition and severe fertility defects. We show that onceZAM-piRNAs are produced in germ cells they counter the invasion. Our study sheds new light on the mechanisms of recognition and regulation of invasive genetic elements, which is essential for the maintenance of genome integrity.

2023-08-25 | GSE235966 | GEO

Germline piRNAs counteract endogenous retrovirus invasion from somatic cells- small RNA

Project description:In metazoan gonads, transposable elements (TEs) mobilization is limited by PIWI-interacting RNAs (piRNAs). These small RNAs originate from specific source loci, the piRNA clusters. piRNAs are known to silence TEs in the cells where they are produced. Endogenous retroviruses (ERVs), a subclass of TEs, pose a particular threat because they are capable of transiting from cell to cell. In this study, we reveal that piRNAs produced locally in germ cells counteract invasion by ERVs arriving from adjacent somatic cells. We reactivated the Drosophila ERV ZAM in somatic gonadal cells by deleting, using CRISPR-Cas9 genome editing, its single copy in the somatic flamenco piRNA cluster, while keeping the piRNA pathway fully functional. Upon reactivation, ZAM invaded the oocytes, resulting in transposition and severe fertility defects. We show that once ZAM-piRNAs are produced in germ cells they counter the invasion. Our study sheds new light on the mechanisms of recognition and regulation of invasive genetic elements, which is essential for the maintenance of genome integrity.

2022-09-30 | GSE213368 | GEO

An epigenetic role for maternally inherited piRNAs in transposon silencing.

Project description:In plants and mammals, small RNAs indirectly mediate epigenetic inheritance by specifying cytosine methylation. We found that small RNAs themselves serve as vectors for epigenetic information. Crosses between Drosophila strains that differ in the presence of a particular transposon can produce sterile progeny, a phenomenon called hybrid dysgenesis. This phenotype manifests itself only if the transposon is paternally inherited, suggesting maternal transmission of a factor that maintains fertility. In both P- and I-element-mediated hybrid dysgenesis models, daughters show a markedly different content of Piwi-interacting RNAs (piRNAs) targeting each element, depending on their parents of origin. Such differences persist from fertilization through adulthood. This indicates that maternally deposited piRNAs are important for mounting an effective silencing response and that a lack of maternal piRNA inheritance underlies hybrid dysgenesis.

| S-EPMC2805124 | biostudies-literature

Germline piRNAs counteract endogenous retrovirus invasion from somatic cells - Total genomic DNA

Project description:In metazoan gonads, transposable elements (TEs) mobilization is limited by PIWI-interacting RNAs (piRNAs). These small RNAs originate from specific source loci, the piRNA clusters. piRNAs are known to silence TEs in the cells where they are produced. Endogenous retroviruses (ERVs), a subclass of TEs, pose a particular threat because they are capable of transiting from cell to cell. In this study, we reveal that piRNAs produced locally in germ cells counteract invasion by ERVs arriving from adjacent somatic cells. We reactivated the Drosophila ERV ZAM in somatic gonadal cells by deleting, using CRISPR-Cas9 genome editing, its single copy in the somatic flamenco piRNA cluster, while keeping the piRNA pathway fully functional. Upon reactivation, ZAM invaded the oocytes, resulting in transposition and severe fertility defects. We show that once ZAM-piRNAs are produced in germ cells they counter the invasion. Our study sheds new light on the mechanisms of recognition and regulation of invasive genetic elements, which is essential for the maintenance of genome integrity.

2022-09-30 | GSE213456 | GEO

A novel epigenetic mechanism in Drosophila somatic cells mediated by Piwi and piRNAs.

Project description:Small noncoding RNAs have emerged as key players in epigenetic regulation. Recently, a novel class of small RNAs that interact with Piwi proteins has been discovered in the mammalian and Drosophila germ line. These Piwi-interacting RNAs (piRNAs) represent a distinct small RNA pathway that is widely thought to function only in the germ line. In this chapter, we review our recent work with our collaborators on the epigenetic function of the Drosophila Piwi protein and its associated piRNAs in somatic cells. This work has revealed a novel epigenetic mechanism mediated by Piwi and its associated piRNAs in somatic cells that might also be applicable to the germ line. On the basis of these results, we propose a "Piwi-piRNA guidance hypothesis" for Piwi/piRNA-mediated epigenetic programming, in which the Piwi-piRNA complex serves as sequence-recognition machinery that recruits epigenetic effectors such as heterochromatin protein 1a (HP1a) to specific sites in the genome to execute epigenetic regulation.

| S-EPMC2810500 | biostudies-literature

The human Piwi protein Hiwi2 associates with tRNA-derived piRNAs in somatic cells.

Project description:The Piwi-piRNA pathway is active in animal germ cells where its functions are required for germ cell maintenance and gamete differentiation. Piwi proteins and piRNAs have been detected outside germline tissue in multiple phyla, but activity of the pathway in mammalian somatic cells has been little explored. In particular, Piwi expression has been observed in cancer cells, but nothing is known about the piRNA partners or the function of the system in these cells. We have surveyed the expression of the three human Piwi genes, Hiwi, Hili and Hiwi2, in multiple normal tissues and cancer cell lines. We find that Hiwi2 is ubiquitously expressed; in cancer cells the protein is largely restricted to the cytoplasm and is associated with translating ribosomes. Immunoprecipitation of Hiwi2 from MDAMB231 cancer cells enriches for piRNAs that are predominantly derived from processed tRNAs and expressed genes, species which can also be found in adult human testis. Our studies indicate that a Piwi-piRNA pathway is present in human somatic cells, with an uncharacterised function linked to translation. Taking this evidence together with evidence from primitive organisms, we propose that this somatic function of the pathway predates the germline functions of the pathway in modern animals.

| S-EPMC4132735 | biostudies-literature

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