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Piwi is a key regulator of both somatic and germline stem cells in the Drosophila testis

ABSTRACT: The Piwi-piRNA pathway is well known for its germline function, yet its somatic role remains elusive. We show here that Piwi is required autonomously not only for germline stem cell (GSC) but also for somatic cyst stem cell (CySC) maintenance in the Drosophila testis. Reducing Piwi activity in the testis caused defects in CySC differentiation. Accompanying this, GSC daughters expanded beyond the vicinity of the hub but failed to differentiate further. Moreover, Piwi deficient in nuclear localization caused similar defects in somatic and germ cell differentiation, which was rescued by somatic Piwi expression. To explore the underlying molecular mechanism, we identified Piwi-bound piRNAs that uniquely map to a gene key for gonadal development, Fasciclin 3, and demonstrate that Piwi regulates its expression in somatic cyst cells. Our work reveals the cell-autonomous function of Piwi in both somatic and germline stem cell types, with somatic function possibly via its epigenetic mechanism. Examination of Piwi-piRNAs in fly testis

ORGANISM(S): Drosophila melanogaster

SUBMITTER: Na Liu

PROVIDER: E-GEOD-68997 | biostudies-arrayexpress |

REPOSITORIES: biostudies-arrayexpress

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Piwi is a key regulator of both somatic and germline stem cells in the Drosophila testis

Project description:The Piwi-piRNA pathway is well known for its germline function, yet its somatic role remains elusive. We show here that Piwi is required autonomously not only for germline stem cell (GSC) but also for somatic cyst stem cell (CySC) maintenance in the Drosophila testis. Reducing Piwi activity in the testis caused defects in CySC differentiation. Accompanying this, GSC daughters expanded beyond the vicinity of the hub but failed to differentiate further. Moreover, Piwi deficient in nuclear localization caused similar defects in somatic and germ cell differentiation, which was rescued by somatic Piwi expression. To explore the underlying molecular mechanism, we identified Piwi-bound piRNAs that uniquely map to a gene key for gonadal development, Fasciclin 3, and demonstrate that Piwi regulates its expression in somatic cyst cells. Our work reveals the cell-autonomous function of Piwi in both somatic and germline stem cell types, with somatic function possibly via its epigenetic mechanism.

2015-05-23 | GSE68997 | GEO

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

PIWI-piRNA pathway mediated transposon repression in Hydra somatic stem cells

Project description:Transposable elements (TEs) can damage genomes, thus organisms employ a variety of mechanisms to repress TE expression. The PIWI-piRNA pathway is a small RNA pathway that represses TE expression in the germline of animals. Here we explore the function of the pathway in the somatic stem cells of Hydra, a long-lived freshwater cnidarian. Hydra have three stem cell populations, all of which express PIWI proteins; endodermal and ectodermal epithelial stem cells are somatic, whereas the interstitial stem cells have germline competence. To study somatic function of the pathway we isolated piRNAs from Hydra that lack the interstitial lineage and found that these somatic piRNAs map predominantly to TE transcripts and display the conserved sequence signatures typical of germline piRNAs. Three lines of evidence suggest that the PIWI-piRNA pathway represses TEs in Hydra epithelial stem cells. First, epithelial knockdown of the Hydra piwi gene hywi resulted in upregulation of TE expression. Second, degradome sequencing revealed evidence of PIWI-mediated cleavage of TE RNAs in epithelial cells using the ping-pong mechanism. Finally, we demonstrated a direct association between Hywi protein and TE transcripts in epithelial cells using RNA immunoprecipitation. Altogether, our data reveal that the PIWI-piRNA pathway represses TE expression in the somatic cell lineages of Hydra, which we propose contributes to the extreme longevity of the organism. Furthermore, our results, in combination with others, suggest that somatic TE repression is an ancestral function of the PIWI-piRNA pathway.

2019-08-07 | GSE135440 | GEO

The RNA Polymerase II subunit RPB-9 directs transcriptional elongation at piRNA loci in C. elegans

Project description:PIWI-interacting RNAs (piRNAs) are genomically-encoded small RNAs that regulate germ cell development and guarantee germline integrity. Mature piRNAs engage Piwi Argonaute proteins to silence complementary transcripts, including transposable elements and endogenous genes. To date, piRNA biogenesis mechanisms are still unclear. Here, we show that the RNA Polymerase II subunit RPB-9 is required to promote transcription elongation at piRNA loci. Through genetic and biochemical experiments, we demonstrate that rpb-9-mediated piRNA production is needed to repress two DNA transposon families and a subset of somatic genes in the C. elegans germline.

2020-12-07 | PXD018657 | Pride

Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila

Project description:In Drosophila, Piwi proteins associate with Piwi-interacting RNAs (piRNAs) and protect the germline genome by silencing mobile genetic elements. This defense system acts in germline and gonadal somatic tissue to preserve germline development. Genetic control for these silencing pathways varies greatly between tissues of the gonad. Here, we identified Vreteno (Vret), a novel gonad-specific protein essential for germline development. Vret is required for piRNA-based transposon regulation in both germline and somatic gonadal tissues. We show that Vret, which contains Tudor domains, associates physically with Piwi and Aubergine (Aub), stabilizing these proteins via a gonad-specific mechanism, absent in other fly tissues. In the absence of vret, Piwi-bound piRNAs are lost without changes in piRNA precursor transcript production, supporting a role for Vret in primary piRNA biogenesis. In the germline, piRNAs can engage in an Aub/Argonaute 3 (AGO3)-dependent amplification in the absence of Vret, suggesting that Vret function can distinguish between primary piRNAs loaded into Piwi/Aub complexes and piRNAs engaged in the amplification cycle. We propose that Vret acts at an early step in primary piRNA processing where it plays an essential role in transposon regulation. These studies show that vreteno (vret) has a role in germline development and primary piRNA regulation in Drosophila. Transposable element expression profiles from Drosophila ovaries mutant for vreteno, piwi and aubergine were compared using genome-wide mRNA expression profiling by Affymetrix GeneChip arrays (Drosophila 2.0). Key targets were validated by qPCR experiments.

2011-09-28 | E-GEOD-30360 | biostudies-arrayexpress

Characterization of active piRNAs and an piRNA machinery in WRR-1 cells deficient for the Hippo pathway (deficient for the warts tumor suppressor) and expressing activated RasV12 (small RNA)

Project description:We have found that oncogenic Ras combined with loss of the Hippo tumour-suppressor pathway reactivates a primary piRNA pathway in Drosophila somatic cells, coincident with oncogenic transformation. In these cells, Piwi becomes loaded with piRNAs derived from generative loci, which are normally restricted to either the germline or the somatic follicle cells. Negating the pathway leads to increases in the expression of a wide variety of transposons and also to altered expression of some protein coding genes. This correlates with a reduction in the proliferation of the transformed cells in culture, suggesting that at least in this context, the piRNA pathway may play a functional role in cancer. Small RNAs cloned from whole cells, piwi-bound small RNAs and long RNA-Seq were performed in wts-RNAi;RasV12 cells to identify piRNAs and gene expression and compared to RasV12 cells, somatic OSS cells, and germline UAS-wts-RNAi;UAS-RasV12 control ovaries. After knock-down of several components of the piRNA machinery in WRR-1 cells (piwi, zuchini, armitage, aubergine, argonaute3) and GFP and/or dsRED control knock-downs, small RNAs were cloned and gene expression profiles (RNA-Seq) were established.

2016-08-01 | E-GEOD-83871 | biostudies-arrayexpress

Characterization of active piRNAs and piRNA machinery in WRR-1 cells deficient for the Hippo pathway (deficient for the warts tumor suppressor) and expressing activated RasV12 (RNA-seq)

Project description:We have found that oncogenic Ras combined with loss of the Hippo tumour-suppressor pathway reactivates a primary piRNA pathway in Drosophila somatic cells, coincident with oncogenic transformation. In these cells, Piwi becomes loaded with piRNAs derived from generative loci, which are normally restricted to either the germline or the somatic follicle cells. Negating the pathway leads to increases in the expression of a wide variety of transposons and also to altered expression of some protein coding genes. This correlates with a reduction in the proliferation of the transformed cells in culture, suggesting that at least in this context, the piRNA pathway may play a functional role in cancer. Small RNAs cloned from whole cells, Piwi-bound small RNAs and long RNA-Seq were performed in wts-RNAi;RasV12 cells to identify piRNAs and gene expression changes compared to RasV12 cells, somatic OSS cells, and germline UAS-wts-RNAi;UAS-RasV12 control ovaries. After knock-down of components of the piRNA machinery in WRR-1 cells ([piwi, zuchini, armitage, aubergine, argonaute3) and GFP and/or dsRED control knock-downs, small RNAs were cloned and gene expression (RNA-Seq) profiles were established.

2016-08-01 | E-GEOD-83843 | biostudies-arrayexpress

RNA elements in precursors instruct directional and processive primary piRNA biogenesis

Project description:PIWI-interacting RNAs (piRNAs) are animal gonad-specific small RNAs that control the activity of transposable elements. Long single stranded RNAs from a variety of sources are substrates for the nebulous primary processing pathway that converts these into thousands of 24-30 nucleotide (nt) piRNAs. How these transcripts are selected as precursors is not known. Here we show that targeting a transcript with PIWI slicer activity of cysosolic Ago3 is sufficient to trigger ~30-nt waves of non-overlapping primary piRNAs in the fly ovarian germline. The generated primary piRNAs are almost exclusively loaded into the nuclear PIWI protein, Piwi. In the fly ovarian somatic environment we find that an RNA fragment from the 5? end of a piRNA cluster is able to direct a heterologous sequence into primary processing. This piRNA trigger sequence (PTS) element drives generation of overlapping piRNAs from the transcript. Both mechanisms proceed with general 5?-3? directionality. We propose that the former pathway serves to link cytoplasmic silencing of a target to nuclear transcriptional repression, while the latter extracts silencing information from a wide variety of genomic sources including piRNA clusters, select protein coding and transposon transcripts. Total or immunoprecipitated small RNAs were purified from transfected BmN4 cells, Drosophila ovarian somatic cells (OSC) and from fly ovaries and high-throughput sequencing libraries were prepared. The mouse testicular RNAs were purified after ribozero treatment.

2015-07-09 | E-GEOD-69102 | biostudies-arrayexpress

Vreteno, a gonad-specific protein, is essential for germline development and primary piRNA biogenesis in Drosophila

2011-09-29 | GSE30360 | GEO

Zebrafish germline small RNAs

Project description:Piwi proteins specify an animal-specific subclass of the Argonaute family, that in vertebrates are specifically expressed in germ cells. We demonstrate that zebrafish Piwi (Ziwi) is expressed in both the male and the female gonad, and is a component of a germline specifying structure, called nuage. Loss of Ziwi function results in a progressive loss of germ cells due to apoptosis during larval development. In animals that have only reduced Ziwi function, germ cells are maintained, but display abnormal levels of apoptosis in adults. In mammals, Piwi proteins have been found to associate with approximately 29-nucleotide long, testis specific RNA molecules, called piRNAs. Here we show that zebrafish piRNAs are present in both ovaries and testes. Furthermore, we show that piRNAs are modified at their 3’ end and that they are produced by a Dicer independent mechanism. Many ovarian piRNAs are derived from transposons, implicating a role for these molecules in the silencing of these repetitive elements in vertebrates. Keywords: high-throughput 454 sequencing sequencing of ~30 nt small RNAs from zebrafish ovaries and testes using 454 technology

2007-04-04 | E-GEOD-7131 | biostudies-arrayexpress

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